Download pelvic appendage myology of the hawaiian honeycreepers

PELVIC
HAWAIIAN
APPENDAGE
MYOLOGY
OF
THE
HONEYCREEPERS (DREPANIDIDAE)
ROBWRTJ. RAIKOW
THts is the first in a seriesof studieson the appendicularmyology
and relationshipsof passerinebirds. Despite the many studiesthat have
been done to clarify relationshipswithin the largest order of birds, the
interrelationshipsof passeriformfamilies are still a matter of great
confusion.Relatively few anatomicalstudieshave beendoneon passerines
as comparedto nonpasserine
orders,and most of these (such as Beecher
1953, Tordoff 1954, Bock 1960) have dealt with the structureof the head
or the pterylosis(Clench 1970). Few studieshave beencarriedout on the
appendicularmusclesof passerinebirds, and most of these (e.g. Berger
1968, Gaunt 1969) have beenlimited to singlespeciesor families. Hudson
(1937) compareda few passerinespecieswith variousnonpasserineforms,
and Stallcup (1954) and Swinebroad(1954) made limited interfamilial
comparisons.Berger (1969) reviewed the present state of knowledgeof
the subjectand emphasized
how little still is knownaboutthe appendicular
myologyof passerines.The needfor new studiesof passerinerelationships
using previously unutilized sourcesof data has been pointed out by a
numberof authorsin recentyears,includingMayr and Amadon (1951),
Beecher (1953), Stresemann (1959), and George and Berger (1966:
229).
The New World nine-primaried oscines (Fringillidae and related
families) constitute a large segmentof oscine forms and encompassa
number of interrelated taxonomicproblems. The present study includes
a largely descriptiveaccountof the myologyof the hind limb in a representativefamily, the I)repanididae, and a subsequentpaper will present
a similar accountof the musclesof the forelimb. Followingthis, hopefully,
a comparativestudy of the entire New World nine-primariedoscineassemblagewill be presented,utilizing an analysis of variations from the
basisof comparisonprovided in the first two studies.
The I)repanididae or Hawaiian honeycreepersare endemic to the
Hawaiian Islands and have been the subjectof much discussionregarding
their originand subsequent
evolution.Nothing hasbeenpreviouslywritten
about their appendicularmyology. The only detailedanatomicalstudy of
this family is an analysisof the feedingmechanismin the genusLoxops
(Richards and Bock 1973). Amadon (1950) reviewed the earlier and
more limited studies of their structure. In the following account each
muscleis describedin detail and illustrated in a representativespecies,
774
The Auk 93: 774-792. October 1976
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HawaiianHoneycreeper
Myology
775
Loxopsvirenswilsoni.This is followedby a comparison
with the other
species
studied.Finally the significance
of thesedata to the problems
of the Drepanididae relationshipsis discussed.
•ATERIAI,S AND •ETI-IODS
The f(•]lowingforms were studied(the numberin parenthesis
showsthe number
of specimens
dissected):Hemignathus
procerus(1), H. wilson{(1), Loxopsmaculata
bairdi (1), L. vlrens wilsonl (3), Psittirostrac. cantans(2), P.c. ultima (2), P.
psittacea(1), Himatione sanguinea(2), Vestiaria coccinea(2), Palmeria dolei (1),
Cirldopsanna (1). The Ciridopsspecimenwas very incompleteand containedonly
a few muscles. Except where specific referenceis made to Ciridops, statementsreferring to a generalconditionin the Drepanididaedo not includethis form.
Dissectionwas doneunder a stereomicroscope
at magnificationsof 6X to 25X, and
the muscleswere made more visible with an iodine stain (Bock and Shear 1972)
that emphasizesdetails of fiber arrangement.
Berger(Georgeand Berger1966) presented
a standardized
nomenclature
for avian
muscles,which I followedin my previouswork (Raikow 1970). In the present
study I have introducedsome changesfrom this systemin accordancewith a new
nomenclature
of aviananatomythat the InternationalCommitteeof AvianAnatomical
Nomenclatureis now developing.This will eventuallybe publishedas Nomina
AnatomicaAvlum (N.A.A.), which it is hoped will stabilizethe nomenclatureof
avian anatomy. The nameschosenare intendedto avoid unsupportedimplicationsof
hornologywith the musclesof mammals,and to be accuratedescriptively.The names
for musclesusedherein have been tentatively adoptedfor the N.A.A. at the time of
this writing. If a namediffers from that givenby Berger (Georgeand Berger1966),
then the older name is given in parentheses
followingthat currentlyadopted. Terms
of direction have also been modified. Cranial means toward the head and replaces
anterior,while caudalmeanstoward the tail and replacesposterior.After eachmuscle
is describedin Loxopsvirens,any variationsin other Drepanididaeare given. If no
suchvariationsare listed,then it may be assumedthat the descriptionfits all the
speciesstudied.
MUSCLE
DESCRIPTIONS
M. •liotibialiscranialis(M. sartorius).--This is the most cranial muscleof
the thigh. It arisesby an aponeurosis
from the caudalpart of the neuralspine
of the fourth dorsalvertebra and the neural spine of the fifth dorsalvertebra,
and is fleshy from the anterior iliac processof the ilium. It insertsby fleshy
fibers on the craniomedial surface of the head of the tibiotarsus and the
medialmarginof the pateIlartendon.The insertionis coveredby the pateIlar
bandof M. gastrocnemius
parsinterna. The muscleis basicallyparallel-fibered,
but as the originis slightlywiderthan the insertion,the fibersconverge
slightly
toward the insertion (Figs. 1, 4).
M. iliotibialislateralis(M. iliotibialis).--Thisflat triangularmusclecovers
the lateralsurfaceof the thigh caudalto M. iliotibialiscranialisand cranialto
M. flexor cruris lateralis. It includeswell-developedpreacetabular,acetabular,
and postacetabular
portions,whichare continuous
with one anotheras in most
passerines.
The muscleoriginates
overmostof its lengthby a broadaponeurosis
from the cranial and caudal illac crestsof the ilium. This aponeurosiscoversthe
776
ROBERT
J.R^ixow
[Auk,
Vol.93
H,
FCi,
lb'
PI3G
GE
PL
bPPD2
FPPD 3
__
b'PD 2
FHI,
TC
PB
Fig.1.Lateral
view
ofthehind
limb
ofLoxops
virens
wilsoni
showing
thesuperficial
muscles.
Abbreviations
forFigs.
1-4:CF,M. caudiliofemoralis
pars
caudo-
femoralis;
EDL,
NI.extensor
digitorum
longus;
FCL,
iVI.flexor
cruris
lateralis
pars
pelvina;
FCLA,
M. flexor
cruris
lateralis
pars
accessorius;
FCM,M. flexor
cruris
medialis;
FDL,iVI.flexor
digitorum
longus;
FHL,M.flexor
hallucis
longus;
FPD2,
iVI.flexor
perforatus
digiti
II; FPD3,
M.flexor
perforatus
digiti
III; FPD4,
M.flexor
perforatus
digiti
IV; FPPD2,
M. flexor
perforans
etperforatus
digiti
II; FPPD3,
October 1976]
Hawaiian HoneycreeperMyology
777
underlyingiliotrochantericus
musclesand extendsdistally to just beyondthe
head of the femur. The origin is fleshy for its caudal1-2 mm. Distally the
centralpart of the muscleis formedby a large aponeurosis
closelyappliedto
the underlyingM. femorotibialisexternus,but fleshy fibers extend nearly
to the insertionat the cranialand caudalmarginsof the muscle.Thesefasciculi
give riseto tendinousfibersthat togetherwith the centralaponeurosis
form the
superficial
layer of the pateIlarligamentthat finallyinsertson the headof the
tibiotarsus(Fig. 1).
M. iliotrochantericus
caudalis(M. iliotrochantericus
posterior).--This large,
roughlyoval-shaped
muscleoccupies
the iliac fossaof the ilium, lying deepto
the aponeuroticorigin of the preacetabular
portion of M. iliotibialislateralis.
Its originis fleshyfrom the concave
surfaceof the iliac fossaand the cranial
iliac crest. The fibers convergeon a short, broad tendonthat insertson the
lateral surfaceof the head of the femur just distal to the trochanter,and
proximalto the insertionof M. iliotrochantericus
medius.The fiber arrangement
is fan-shaped,
with the longestfiberspassingfrom the cranialmarginof the
cranialiliac crest,and progressively
shorterfibersarisingalongthe dorsaland
ventralmarginsof the musclebelly from the cranialtowardthe caudalaspect
of the fossa (Fig. 2).
M. iliotrochantericus
cranialis(M. iliotrochantericus
anterior).--The origin
is from the lateroventralmargin of the preacetabularilium, cranialto that of
M. iliotrochantericus
mediusand deep to M. iliotrochantericus
caudalis.The
muscle inserts on the craniolateral surface of the femur distal to the insertion of
M. iliotrochantericus medius and between the heads of Mm. femorotibialis
externusand femorotibialismedius. Although superficiallythe muscleappears
parallel-fibered,
it is actuallyunipennate.Most of the fibersarisenot directly
from the ilium, but from an aponeurosis
that extendsover the proximalonethird of the lateral surfaceof the musclebelly. Most of the fibers do not insert
directly onto the femur, but via an aponeurosis
that extendsover the distal
one-thirdof the medial surfaceof the belly (Figs. 2, 3, 4).
M. iliotrochantericusmedius.--This tiny muscle has a fleshy origin from
the ventralateraledgeof the ilium caudalto the originof M. iliotrochantericus
cranialis.It insertsby meansof a short,flat tendonon the craniolateral
surface
of the femur proximalto the insertionof M. iliotrochantericus
cranialisand
M. flexor perforans et perforatus digiti III;
FTED, M. femorotibialisexternus pars
distalis; FTEP, M. femorotibialisexternuspars proximalis;FTI, M. femorotibialis
itnernus;FTM, M. femorotibialismedius;GE, M. gastrocnemius
parsexterna;GI, M.
gastrocnemius
pars interna; GSVI,M. gastrocnemius
pars intermedia;IC, M. iliotibialis
cranialis;IF, M. iliofibularis;II, M. iliofemoralis
internus;IL, M. iliotibialislateralis;
ISF, M. ischiofemoralis;ITC, M. iliotrochantericus
caudalis; ITCR, M. iliotrochantericuscranialis; ITM, M. iliotrochantericusmedius; OM, M. obturatorius
medialis;PB, 3/1. peroneusbrevis; PBG, patellar band of M. gastrocnemius;
PIFC,
M. pubischiofemoralis
pars cranialis; PIFCD, M. pubischiofemoralis
pars caudalis;
PL, M. peroneuslongus;T, tibial cartilage;TC, M. tibialis cranialis.
778
ROBERTJ. IL•ZKOW
[Auk, Vol. 93
17'(;
ITCR
lb'
F731
ISb'
FTEP
C'b'
b'C.'11
b'Cl,
bL'l,.t
b•PPD3
G. II
FPPD •
b 7•'I) 2
TC
PB
FPD4
b7'D2
b 7•PI) 2
b7)l,
b7•1) 4
hi'D3
hDL
b7'1'l) 3
Fig. 2. Lateral view of the hind limb of Loxops vlrens wilsoni showing a second
layer of muscles. The following muscles,shown in Fig. 1, have been removed: M.
iliotibialis cranialis, M. iliotibialis lateralis, M. flexor cruris lateralis, proximal portion,
M. peroneuslongus,M. gastrocnemius
pars externa. Abbreviationsunder Fig. 1.
October1976]
HawaiianHoneycreeper
Myology
779
ITCR
ITAI
PIFC
PII•'CD
FC, I1
__
__
(;,11
FI)I,
Fig. 3. Lateralview of the hind limb of Loxopsvirenswilsonishowinga third
layer of muscles.The followingmuscles,shownin Fig. 2, have been removed:
3/1.iliotrochantericus
caudalis,
3/1.femorotibialis
externus,
3/1.femorotibialis
medius,
3/1.iliofibularis,
3/1.caudiliofemoralis
parscaudofemoralis•
3/1.flexorcrurislateralis,
3/1.
flexorperforans
et perforatus
digiti II, M. flexorperforans
et perforatus
digiti iii,
3/1.flexorperforatus
digiti iV• 3/1.tibialiscranialis,3/1.peroneus
brevis.Abbreviations
under Fig. 1.
780
Roe•a'r J. R^•xow
[Auk, Vol. 93
distal to the insertion of M. iliotrochantericuscaudalis. It is nearly parallelfibered, but is slightly wider at the origin than at the insertion (Figs. 3, 4).
M. femorotibialisexternus.--Themain part of this muscle(pars proximaIfs)
has a fleshy origin from the lateral and craniolateral surfacesof the femur,
beginningproximallyat the level of the insertionof M. ischiofemoralis.Somewhat distal to the insertion
of M.
iliotrochantericus
cranialis it is fused for its
entire length with M. femorotibialis medius. A strong tendinoussheet arises
on the distal half of the muscle'ssurface and continuesdistally as the lateral
part of the patellar tendon, which inserts on the head of the tibiotarsus. A
deep distal head (pars distalis) arises from the caudolateralsurface of the
distal half of the femur and joins the proximalhead, forming a deeperlayer of
the patellar tendon (Fig. 2).
M. femorotibialismedius.--This is the central and cranial portion of the
femorotibialiscomplex. It arises fleshy from the cranial surface of nearly
the entire lengthof the femoralshaft. It is fusedwith M. femorotibialisexternus
alongthis lateral marginfor its entire lengthexceptthe proximal2-3 mm. The
insertionis on the proximal face of the patella by both fleshy and tendinous
fibers (Figs. 2, 4).
M. femorotibialisinternus.--This arises from the medial surface of the
femur, primarily by fleshy fibers, but also by a weak aponeurosis
alongits
caudalborder. It has two heads. The proximalhead arisesfrom the proximal
one-half of the femoral shaft, beginningslightly distal to the insertionof M.
iliofemoralis internus. The distal head arises from the distal half of the femur
just proximalto the mediancondyle. The two headsare not clearly separate
at their origins,but insert by adjacentflat tendonson the medialside of the
head of the tibiotarsus,and are unipennatein fiber arrangement(Fig. 4).
M. iliofibularis(M. bicepsfemoris).--This large,roughlytriangularmuscle
lies on the caudolateralsurfaceof the thigh deepto M. iliotibialislateralis. It
arisesby an aponeurosis
from the cranialiliac crestdorsalto the acetabulum
and
from the cranial 3 mm of the caudaliliac crest,the latter part of the origin
beingfleshy. The musclenarrowsdistallyto form a stout tendonthat passes
throughthe bicepsloop,continues
medialto the tendonof originof the lateral
head of M. flexor hallucislongusand M. flexor perforatusdigiti II, and inserts
on the caudolateralsurfaceof the fibular shaft. In superficialappearancethe
fiber architectureof the muscleappearslargely fan-shaped,but dissectionof
the belly showsthat it actuallyapproaches
a bipennateconditionas the tendon
of insertionextendssomeway into the belly,with fibersinsertingon it cranially
and caudally.
The bicepsloop has three arms. The proximalfemoralarm ariseson the
craniolateral surface of the femur about 2 mm from the distal end of the
bone. The distal femoral arm arises on the caudolateral surface of the femur
togetherwith the tendinousorigin of M. gastrocnemius
pars externa. The
fibular
arm arises from
the craniolateral
surface of the fibula
2 mm from
the proximal end of the fibula (Fig. 2).
M. flexor cruris lateralis (M. semitendinosus).--This
strap-shaped,
parallelfibered musclearises fleshy from the caudal end of the caudal iliac crest and
October1976]
II
O•ll
t'11•c
PIFCI)
Hawaiian HoneycreeperMyology
781
17:11
I7L'R
IC
- F7ZII
P'77
I:C. 11
GI
(;,11
EDL
Fig.4. Medialviewof the hindlimbof Loxopsvirenswilsoni.Abbreviations
under
Fig. 1.
tendinously
fromthefirstseveral
caudal
vertebrae.
Distallythebellyisbisected
by a tendinous
raphethat separates
the mainpart (parspdvina)frompars
accessorius
(accessory
semitendinosus).
The rapheextends
beyond
themuscle
in
two branches.One branchbinds M. flexor cruris lateralis to the middle of M.
782
ROBERTJ. l•xxow
[Auk, Vol. 93
gastrocnemius
pars intremedius,while the other joins the tendon of insertionof
M. flexor cruris medialis. Pars accessoriusextends cranioventrally from the
raphe and inserts fleshy on the distal one-fourth of the shaft of the femur
proximal to the external condyleand superficialto M. pubischiofemoralis,
and
medially in the popliteal area of the femur (Figs. 1, 2).
M. caudiliofemoralis
(M. piriformis).--This musclehas two parts in many
birds, pars caudofemoralis
and pars iliofemoralis,but only the former normally
occursin passerines.It is a flat, spindle-shapedmusclethat arsiesby a short
(2 mm) tendonfrom the caudolateralmarginof the pygostyle.It passescraniad
deep to M. iliofibularis and superficial to Mm. flexor cruris medialis, ischiofemoralis, and pubischiofemoralis.It inserts by a short, flat tendon on the
caudalsurfaceof the femur distal to the insertionof M. ischiofemoralis(Fig. 2).
M. ischiofemoralis.--Thislarge, fan-shapedmuscle has a fleshy origin from
the lateral
surface of the ischium caudal to the ilioischiadic
fenestra and from
the ventral surfaceof the laterally projectingcaudaliliac crest. At its caudoventral margin the origin borders the cranial half of the origin of M. flexor
cruris medialis,and the main part of the belly lies superficialto the origin
of M. pubischiofemoralis
pars cranialis. The aponeurosis
of insertionariseson
the lateral surfaceof the distal half of the belly; the muscleis thus unipennate.
The aponeurosis
convergesto a flat tendon0.5 mm wide that insertson the
lateral surface of the femur distal to the insertion of M. iliotrochantericus medius
(Figs. 2, 3).
M. flexor cruris medialis (M. semimembranosus).--This
parallel-fibered,
strap-shapedmusclelies deepin the caudalregionof the thigh. It arisesfleshy
from the caudolateral surface of the ischium caudal to the origin of M.
pubischiofemoralispars cranialis and dorsal to the ischiopubic fenestra. The
musclepassesdistally to insert on the proximomedialsurfaceof the tibiotarsus
by a broad, flat tendon. This tendon is joined by that of M. flexor cruris
lateralis,as described
aboveunderthe discussion
of that muscle(Figs. 1, 2, 3, 4).
M. pubischiofemoralis(M. adductor longus et brevis).--As in passerines
generally, this has two distinct parts, pars cranialis and pars caudalis,which
apparently correspondto pars lateralis and pars medialisrespectivelyin nonpasserines.
Pars cranialis (pars anterior) is the larger of the two muscles. It has a
semitendinous
origin from the ventrolateralmarginof the ischiumbeginningat
the caudaledgeof the obturatorforamenand extendingcaudallyabouthalf the
length of the ischium. It is a parallel-fibered,strap-shapedmuscleand has a
fleshy insertion on the caudal face of the distal half of the femoral shaft. The
area of insertion extends from about the level of the insertion of M. caudilio-
femoralisproximally,to the proximalend of the internalcondyledistally. Along
its caudalmargin,especiallyin the proximalhalf of the belly, this musclelies
superficialto the cranial margin of pars caudalis.
Pars caudalis(pars posterior) arisesby a flat aponeurosisfrom the ventrolateral surfaceof the ischiumbetweenthe origins of M. pubischiofemoralis
pars cranialisand M. flexor cruris lateralis. This aponeurosis
passesdistally
superficialto the membraneoccupyingthe ischiopubicfenestra,and the belly
October 1976]
Hawaiian Honeycreeper Myology
783
of the musclearisesat about the level of the pubis. The parallel-fiberedbelly
extendsdistally and fuseslooselyto the craniodorsalsurfaceof the cranial half
of the belly of M. gastrocnemius
pars intermedia. It then turns cranially and
has a largely tendinousinsertionon a tubercle on the proximal side of the
internal condyleof the femur in commonwith the origin of M. gastrocnemius
pars intermedia(Figs. 3, 4).
The area of insertion of pars cranialis extends about two-thirds the
length of the femoral shaft in Psittirostra.
M. obturatoriuslateralis (M. obturatorexternus).--This musclehas separate
dorsal and ventral bellies. Pars dorsalisis a short (3 mm X 1 mm) parallelfibered muscle. The origin is fleshy from a small area on the lateral surface
of the ischium just caudodorsalto the obturator foramen and on the ventral
margin of the ilioischiadicfenestra. The musclepassescraniallysuperficialto
the tendon of M. obturatorius medialis and has a fleshy insertion on the
femur just cranial to the insertionof the obturatoriusmedialistendon, onto
which a few fibers also insert. Pars dorsaliswas presentin all forms studied,
includingCiridopsanna. Pars ventralis is a compactmass of short, parallel
fibers that arise fleshy from the lateral surface of the ischium along the
cranioventralborder of the obturator foramen and have a fleshy insertionon the
caudomedialsurfaceof the femur just distal to the insertionof M. obturatorius
medialis.
M. obturatoriusmedialis (M. obturator internus).--This flat, leaf-shaped,
bipennatemuscle occupiesthe ischiopubicfenestra medial to the ischiopubic
membrane. It has a fleshy origin from the ischiumand pubis forming the
rim of the fenestra. The fibers convergeon two central tendonsthat fuse
near the obturatorforamen. The singletendonthus formedpassesout through
the obturator foramen and inserts on the caudolateral surface of the head of
the femur in conjunctionwith M. obturatoriuslateralis as describedabove
(Fig. 4).
M. iliofemoralisinternus (M. iliacus).--This tiny, strap-shaped,parallelfiberedmusclehas a fleshyorigin from the ventral edgeof the ilium caudomedialto the originof M. iliotrochantericus
medius. It passescaudoventrally
to a fleshyinsertionon the medial sideof the femur proximalto the originof
M. femorotibialisinternus (Fig. 4).
M. gastrocnemius.--This
muscleis composedof three separatebellieswith
a commontendonof insertion. Pars externaarisesby a broad, flat tendonfrom
the caudolateralsurface of the distal end of the femur just proximal to the
externalcondyle.This tendonis fused to the lateral arm of the underlying
bicepsloop. The muscleextendsabout one-half the length of the crus and
ends in a tendon that is joined medially by that of pars intermediaand
pars interna to form the common tendon of insertion. The tendon of origin
spreadsto form the medial surface of the muscle,while the tendonof insertion
arises as an aponeurosis over the lateral surface. The fibers pass from the
former to the latter, so the muscleis essentiallyunipennatein construction.
Pars intermediais the smallestpart of M. gastrocnemius,
extendinglessthan
one-thirdthe length of the crus. It is a flattened,parallel-fiberedmusclethat
784
ROBERTJ. RAIKOW
[Auk, Vol. 93
arises tendinouslyfrom the proximocaudalsurface of the internal femoral
condyle,whereit is closelyassociated
with the insertionof M. pubischiofemoralis
pars caudalis.Distally it endsin an aponeurosis
that joinswith the tendonsof
the other two bellies to form one tendon of insertion. On its lateral surface it
is joinedby the tendonseparatingthe two parts of M. flexor crurislateralis.
Pars internais the mostsuperficialmuscleon the medialsurfaceof the crus.
It arisesby two distinctheads. The anteriorhead arisesin part from the
inner cnemialcrest,while a band of fibers (the patellarband) extendsaround
the cranialsurfaceof the knee,arisingfrom the pateIlartendon. This portion
overliesthe insertionof M. iliotibialiscranialis.A smallpart of parsinterna
wasretainedin the incomplete
specimen
of Ciridopsanna,showing
that a pateIlar
bandis presentasin the otherformsstudied.Bothpartsof the originarefleshy.
The posteriorhead of pars interna arisesfrom the medialsurfaceof the head
of the tibiotarsus.The two headsfuseand the commonbelly extendsdistally.
It givesrise to a tendonthat joins with thoseof pars intermediaand pars
externato form the tendonof insertion. This passesover the tibial cartilage,
is lightly boundto the hypotarsus,
and then has a long insertionalongthe
plantar ridge of the tarsometatarsus.
It is alsoboundinto the fascialcovering
overlyingthe flexortendonson the plantarsurfaceof the tarsometatarsus
(Figs.
1, 2, 3, 4).
M. tibialis cranialis(M. tibialis anterior).--This lies on the cranial surface
of the crus deep to M. peroneuslongus. It has two bipennateheads. The
tibial head has a fleshy origin from the lateral surfaceof the inner cnemial
crest, the medial surfaceof the outer cnemialcrest, and the rotular crest
superficialand cranial to the origin of M. extensord/gitorumlongus. The
femoral head arisesby a short, stout tendon from the apex of the external
condyleof the femur. The two headsfuse just proximalto the formationof
the commontendon of insertion and extend slightly more than half the length
of the crus. The tendon passesdistally along the cranial surface of the
tibiotarsus,passesbeneath the ligamentumtransversum,and inserts on the
dorsalsurfaceof the tarsometatarsus
(Figs. 1, 2, 4).
M. extensordigitorumlongus.--Thismuscleoccupiesthe craniomedialsurface of the tibiotarsusdeepto M. tibialis cranialis.The belly extendsabouthalf
the length of the crus. The origin is fleshy from the medial side of the inner
cnemial crest, the base of the outer cnemial crest, and the rotular crest and
head of the tibiotarsusbetweenthe two cnemialcrests,as well as from the
shaft of the proximal one-fourthof the tibiotarsus. The muscleis fan-shaped
and unipennate,the fibers convergingon a strongtendonthat arisesalongthe
cranial surface of the belly. The tendon passesbeneath the ligamenturn
transversumdeep to the tendon of M. tibialis cranialis, beneath a bony
bridge,and then crossesthe intertarsaljoint. At the proximalend of the
tarsometatarsus
it passesthrougha thin bony canaland then proceedsdistally
alongthe dorsalsurfaceof the tarsometatarsus,
at the distal end of which it
dividesinto threebranches,oneto eachof the cranialdigits.
The branchto digit II bifurcates,
the medailbranchinsertingon the dorsal
surfaceof the proximalend of the secondphalanx,while the lateral branch
October 1976]
I-Iawaiian HoneycreeperMyoIogy
785
insertson the proximodorsal
surfaceof the ungualphalanx.There are small
sesamoids
at both insertions.The branchto digit III dividesinto lateral and
medialtendonsthat interconnectin a complexway (see Fig. 3) with insertions
on the proximalendsof the second,third, and ungualphalanges.The branch
to digit IV bifurcates,the lateral branchinsertingon the ungualphalanxin
association
with an automaticextensorligament. The medialbranchbifurcates
and insertson the basesof the third and fourth phalanges.
In Loxopsmaculata,
Psittirostra
cantans,
Himationesanguinea,
Palmeriadolei,
and Vestiariacoccinea
the bellyis the samelengthasin Loxopsvirens,whilein
the other formsit is abouttwo-thirdsthe lengthof the crus(Figs. 3, 4).
M. peroneus
longus.--M.peroneus
longusoccupies
the craniolateral
surface
of the crussuperficial
to M. tibialiscranialis,
whichit almostcompletely
covers.
It has a fleshyoriginfrom the inner cnemialcrest,the rotularcrest,and the
outercnemialcrestof the tibiotarsus,
andan aponeurotic
originfromthe medial
surface of the head of the tibiotarsus. Some fibers are also associatedwith the
fascialcoveringof the underlyingM. tibialis cranialis.The bipennatemuscle
extendslessthan half the lengthof the crusand givesrise to a tendonthat
passesalongthe lateral surfaceof the tibiotarsusand bifurcatesabout 3 mm
proximalto the externalcondyle.One branchinsertson the proximolateral
cornerof the tibial cartilage.The other passesacrossthe intertarsaljoint
superficial
to theperoneus
brevistendonandpasses
to the lateroplantar
surface
of the tarsometatarsus,
whereit joinsthe tendonof M. flexorperforatusdigiti
III
(Figs. 1, 4).
M. peroneusbrevis.--Thismusclelies on the lateral surfaceof the crusjust
caudalto the tibial headof M. tibialis cranialis.It has a fleshyoriginfrom the
caudalmarginof the outercnemialcrest,just caudalto the originof the tibial
headof M. tibialiscranialis.This tibial headpassesdistallysuperficialto the
femoralheadof M. tibialiscranialisandjoinsa fibularhead,whicharisesfrom
the craniolateralsurfaceof the fibular shaft beginningjust distal to the point
of insertionof M. iliofibularis.The belly extendsa little morethan half the
lengthof the tibiotarsus
andgivesriseto a tendonthat passes
distallylateralto
the tendonof M. tibialiscranialis.It passes
beneatha fibrousloopjustproximal
to the lateralcondyle
of thetibiotarsus,
thenwidens
andpasses
laterallyof the
lateral condyleto insert on the proximalend of the tarsometatarsus.
The musclewas identical in all Drepanididaeexamined,but it was not seen
in Ciridops.A tibial head has apparentlynever been describedin birds, and
is not mentionedin Georgeand Berger (1966). It is an importanttaxonomic
characterin the New World nine-primariedoscines,and will be considered
morefully in a laterpaperon the relationships
of thisassemblage
(Figs.1, 2).
M. flexorperforanset perforatusdigiti III.--This musclelies on the lateral
surfaceof the crus caudalto M. peroneuslongusand cranialto M. flexor
perforatusdigitiII. Its originis partly concealed
beneathM. flexorperforans
et perforatusdigiti II. The belly is formedby fibers converging
from two
distinctheads. The cranialhead arisesprimarily fleshy from the outer cnemial
crestof the tibiotarsusand the adjacentpatellartendon.The caudalheadarises
by an aponeurosis
fromtheproximalpart of thelateralfemoralcondyle,
together
786
ROBEaTJ. l•xKow
[Auk, Vol. 93
with M. flexorperforatusdigiti II and M. flexorperforanset perforatusdigiti
II. The proximalhalf of the muscleis bipennate,as fibers from the two points
of origin convergeon a centraltendon. Distally the musclenarrowsas the
componentfrom the caudal head ends, and only the cranial head continues.
This part is thus unipennate.
The muscleextendsdistally about half the length of the tibiotarsus.It gives
rise to a tendon that passesthrough a canal in the medial part of the tibial
cartilageand then through the posteromedialcanal of the hypotarsus.It continues distally along the plantar surface of the tarsometatarsusto the plantar
side of digit III. Here it ensheathesthe tendon of M. flexor digitorum longus,
and these two tendonsperforate the tendonof M. flexor perforatusdigiti III.
The tendon of M. flexor perforanset perforatus digiti III then bifurcates, the
tendon of M. flexor digitorumlonguscontinuingdistally between the branches.
The two branchesinsert on the lateral and medial sides, respectively,of the
proximoplantarend of the third phalanx of digit III (Figs. 1, 2).
M. flexor perforanset perforatusdigiti //.--This small (7 mm) musclelies
on the lateral surfaceof the crusjust caudalto M. flexor perforanset perforatus
digiti III. It has a fleshy origin from the caudoproximalcorner of the lateral
femoral condyle, just distal to the origin of M. gastrocnemiuspars externa.
The fiber arrangementis nearly parallel, but approachesbeing unipennate
as the fibers insert into the tendon of insertion which arises on the caudolateral
surface of the belly. The fine tendon passesdistally through the median part
of the tibial cartilageand the posteromedial
canalof the hypotarsus.It proceeds
alongthe plantar surfaceof the tarsometatarsus
to digit II, whereit bifurcates.
The main insertionis on the medial surface of the base of phalanx 2, while
an elasticligamentinsertssubterminallyon the distoplantarsurfaceof phalanx
1 of digit II. The belly appearsslightly elongatedin Psittirostra c. cantans
(Figs. 1, 2).
M. flexor perforatusdigiti IV.--This long, spindle-shaped
musclelies on the
caudal surface of the crus caudomedialto M. flexor hallucis longus and
lateral to M. flexor perforatus digiti III. It has a partly fleshy origin from the
intercondyloidregion of the femur in commonwith the medial head of M. flexor
hallucislongusand M. flexor perforatusdigiti III. In addition,somefibers arise
directly from the tendinous origin in common with the latter muscle. The
belly extendsdistally about half the length of the crus. The tendon of insertion arises as an aponeurosison the caudolateralsurface of the belly. The
fibers insert into this aponeurosisfrom beneath so the fiber arrangementis
essentiallyunipennate. The tendon proceedsdistally through the tibial cartilage
loosely ensheathedby the tendon of M. flexor perforatus digiti III. The two
tendonscontinuethrough the posterolateralcanal of the hypotarsusand along
the plantar surfaceof the tarsometatarsus.At the base of digit IV the tendon
of M. flexor perforatus digiti IV bifurcates and is perforated by the tendon
of M. flexor digitorumlongus. The lateral branch of the tendon insertsat the
base of phalanx 2 of digit IV, while the larger median branch inserts at the
base of phalanx3. The belly extendsabout three-fourthsthe length of the crus
in Psittirostra and Hemignathus(Fig. 2).
October 1976]
Hawaiian HoneycreeperMyology
787
M. flexor perJoratus
digiti ///.--This musclearisesfrom the intercondyloid
regionof the femur by a tendonin commonwith M. flexorperforatusdigiti
IV and M. flexorhallucislongus.It lies medialto M. flexorperforatusdigiti
IV andextends
abouthalf thelengthof thecrus.The fiberspassfromthetendon
of origin on its lateraI surfaceto an aponeurosis
on the medialsurfacefrom
which the tendon of insertionarises; it is thereforebasicallyunipennatein
form. The tendonproceedsthroughthe tibial cartilageand the posterolateral
canalof the hypotarsus
cranialto and looselyensheathing
the tendonof M.
flexor perforatusdigiti IV. Beyondthe hypotarsusthe two tendonsdiverge,
the tendonof M. flexorperforatusdigiti III beingjoinedby the longbranch
of the tendonof M. peroneuslongus. At the base of digit III the tendon
bifurcatesto allowpassage
of the tendonsof M. flexorperforanset perforatus
digitiIII andM. flexordigitorum
longus.The twobranches
insertonthe medial
and lateral cornersrespectively,
of the baseof phalanxl of digit III. In
Hemignathus
and Psittirostrathe belly extendsaboutthree-fourths
the length
of the crus (Fig. 2).
M. flexorper•oratusdigiti//.--This small,spindle-shaped
musclearisesby an
aponeurosisfrom the caudal surface of the external fernoral condyledistal
to the originof M. gastrocnemius
parsexterna,sharingan aponeurosis
of origin
with thelateralheadof M. flexorhallucislongus,
andalsoby a shortaponeurosis
from the neck of the fibula. The belly extendsabouthalf the lengthof the
crusand givesrise to a tendonthat passesthroughthe lateralpart of the
tibial cartilage,throughthe middlecanalof the hypotarsus,
andcontinues
along
the plantarsurfaceof the tarsometatarsus.
It thenpasses
througha canalin
the ligamentsat the baseof digit II and insertson the proximomedial
cornerof
the baseof phalanx1 of digit II. It is not perforatedby the tendonsof either
M. flexor perforanset perforatusdigiti II or M. flexor digitorumlongusas
in some birds (Figs. 1, 2).
M. plantaris.--Thisis absent in Loxops virens wilsoni. The foliowing
description
is for Psittirostrac. cantans.This tiny (4 mm) triangularmuscle
arisesfleshyfrom the caudomedial
surfaceof the headof the tibiotarsus
just
medial to the medial head of M. flexor digitorumlongus. The fine tendon
passes
distallyand insertson the proximomedial
cornerof the tibial cartilage.
M. plantarisis also absentin Himationesanguinea,
?almeriadolei, and
Vestiaria
coccinea,
but is present
in the otherformsstudied,
thoughit is poorly
developedin Loxopsmaculata.
M. flexor hallucislongus.--Thismusclehas three heads. The small lateral
head arises from the caudolateralsurface of the proximal end of the lateral
fernoralcondyleby meansof an aponeurosis
closelyconnected
to the aponeurosis
of origin of the intermediatehead and M. flexor perforatusdigiti II. This
aponeurosis
passes
lateralto the iliofibularistendon,at whichpointthe belly
of the lateralheadarises.This belly fuseswith the intermediateheadnear the
end of the muscle. The intermediate head arisesby an aponeurosisfrom the
distal end of the femur, partly fuseswith the origin of the lateral head, but
passesmedialto the iliofibularistendon.The medialheadarisesfleshyfrom
the intercondyloid
regionof the femur. Somefibersalsoarisefrom the medial
788
ROBeRt J. R^•cow
[Auk, Vol. 93
side of the cranial end of the aponeurosisof origin of the intermediatehead.
Otherwisethe two headsare separatefor mostof their length,but fuse near the
distal end of the muscle.
The muscleis bipennate. The fibers of the medial head convergelaterally,
and thoseof the other two headsconvergemedially onto the tendonof insertion.
The muscleextendsabout half the length of the crus,givingrise to a tendonthat
passes through a deep canal in the tibial cartilage, and then through the
anterolateralcanal of the hypotarsus.The tendon passesdistally along the
plantar surfaceof the tarsometatarsus,crossingto the medial side superficialto
the tendonof M. flexor digitorumlongus. No vinculum connectsthesetendons.
The tendon then passesbetweenthe tarsometatarsusand metatarsal I. Passing
around the trochlea of metatarsal I it is ensheathedin a pulley arising from
the tendon of M.
flexor
hallucis brevis.
The
tendon inserts on the base of
the ungual phalanx of the hallux. An elastic vinculum arises from the inner
surface of the tendon at about the level of the middle of the first phalanx and
inserts on the plantar surface of the first phalanx just proximal to its distal
articular surface. Before doing so it gives rise to a thin branch that inserts on
the cartilaginouspad betweenthe two phalangesof the hallux. In Psittirostra
the belly is slightly elongated(Fig. 1).
M. flexor digitorumlongus.--This is the deepestmuscleon the caudalsurface
of the crus. It arises fleshy by two heads,the lateral one from the caudal
surface of the head of the fibula and the medial one from the caudal surface of
the head of the tibiotarsus.No femoral head is presentas has been found in a
few passerines
(Georgeand Berger1966: 450-451). The two headsfusedistally
into a single belly, from which a strong tendon arises. The muscle is thus
bipennate. The belly extendsnearly two-thirds the length of the crus. The
tendon proceedsdistally througha deep, medial portion of the tibial cartilage
and then through the anteromedialcanal of the hypotarsus. It passesalong the
plantar surfaceof the tarsometatarsus,passingdeep to the tendon of M. flexor
hallucislongus.The distal two-thirdsof the tendonis rigid, presumablyossified.
At the level of metatarsal I the tendon divides into three branches,one passing
along the plantar surface of digits II, III, and IV respectively. The branch
to digit II insertsat the baseof the ungual phlanx and, by an elastic vinculum,
near the distal end of the secondphalanx. The branch to digit III insertson
the ungualphalanxand by elasticbandson the distal end of phalanx3 and on
the cartilaginouspad at the proximalend of phalanx3. The branchto digit IV
insertson the ungualphalanxand by elasticbandson the distalend of phalanx
4 and on the pad at the base of phalanx 4.
The muscle is generally similar in all speciesexcept that in both races of
Psittirostra cantans and in Palmeria dolei the elastic band to the cartilaginous
pad at the baseof phalanx4 of digit IV is absent(Figs. 2, 3).
M. flexor hallucisbrevis.--This fine strand of musculartissuearisesfrom the
medial surface of the hypotarsusand extendsdistally along the medioplantar
surfaceof the tarsometatarsus.A fine tendonis formed that passesdistally and
ends by being incorporated into the connectivetissue sheathing the tendon
of M. flexor hallucislongusas this passesover the trochlea of metatarsalI. I
October 1976]
Hawaiian HoneycreeperMyology
789
couldnot demonstratethe existenceof this musclein Loxopsmaculata,perhaps
becauseit is so small and the specimenwas poorly fixed. In Psittirostra
psittaceathe musclearisesby a tendon5 mm long rather than by the typical
fleshy origin.
M. extensorhallucislongus.--This muscleincludesproximal and distal heads.
The proximalheadis a tiny, parallel-fiberedmusclearisingon the craniomedial
surfaceof the tarsometatarsus
about 1 mm distal to its proximal articular
surface.It passesdistallymedialto the tendonsof M. tibialis cranialisand
M. extensordigitorumlongus.About halfway alongthe tarsometatarsal
shaft
the 10 mm long belly givesrise to a fine, hairlike tendonthat curvescaudomediallyand passesto the dorsalsurfaceof the hallux. It continues
alongthe
dorsalsurfaceof the proximalphalanx,passesbetweenthe armsof an automatic
extensorligament,and insertswith the latter at the baseof the ungualphalanx.
A distal head has been describedin a few nonpasserine
birds (Georgeand
Berger 1966: 454-455), but apparentlyhas not previouslybeen found in any
passerine.
It is exceedingly
tiny and I discovered
it only after stainingwith
iodine (Bock and Shear1972). This distalheadis a fan-shaped
muscleabout
3 mm long. It arisesfrom the medial surfaceof the distal end of the shaft
of the tarsometatarsus
just proximalto the first metatarsal.It passesdistally
alongsidethe tendonof the proximalheadand insertsinto the joint capsulebetween metatarsal I and the proximal phalanx of the hallux.
M. lumbricalis.--Thissmall, strap-shaped
musclelies deep in the plantar
surface of the foot. It arises from the tendon of M. flexor digitorum longus
just proximalto the point wherethat tendondivides,and insertson the joint
pulleys of digits III and IV.
DISCUSSION
The outstandingfeature evident from the muscledescriptions
given
aboveis the generaluniformityof the hindlimb muscles
in the Drepanididae. The differencesare relativelyminor considering
the great diversity
in the feedingapparatus
in thesespecies.Loxops,Himatione,andPalmeria
haveshort,slightlydecurvedor straightbills and feedby gleaninginsects
from tree surfaces,as well as on nectar. Vestiariaand Hemignathus
have long, crescent-shaped
bills for probing,and Psittirostrahas a short,
conical,finchlikebill. The evolutionof the feedingapparatusin the
Drepanididaeis a classicexampleof adaptive radiation (Bock 1970,
Richardsand Bock 1973), and it is noteworthythat this radiationin the
feedingmechanismwas not accompanied
by a comparableevolutionin
the hind limb musculature. Neverthelesssomevariations may be noted
(Table 1).
The extensorof the digits (M. extensordigitorumlongus)and several
flexorsare significantlyenlargedin Psittirostraand Hemignathusas compared to Loxops,Himatione,Palmeria,and Vestiaria. While a precise
analysisof the biomechanical
characteristics
is not possiblewith the
79O
RObeRT J. RAIKOW
TABLE
[Auk, Vol. 93
1
MAJOR VARIATIONSIN TIlE HIND LIMB MYOLOGY OF DREPANIDIDAE
•t
Muscles
Species
EDL
FPD3
FPD4
FHL
Loxops virens wilsoni
L. maculata bairdi
q-
Psittlrostrac. cantans
P.c. ultima
P. psittacea
Hemlgnathus wilsonl
H. procerus
Himatione sanguinea
Plantaris
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
qq-
*
-{qq-
Palmeria
dolei
-
Vestiaria
coccinea
-
x* means that the muscle belly is significantly longer relative to the length of the crus than in
L. virens; q- means that the muscle is present; - means that the muscle is absent. Abbreviations:
EDL, M. extensor digitorum longus; FPD3, M. flexor perforatus digiti III; FPD4, M. flexor
perforatus digiti IV; FHL, M. flexor hallucis longus.
limited material available, probably the strength of the grip of the foot
is increasedby these enlarged flexor muscles; the enlargementof the
extensormay be correlatedwith this in someway. This changemay be
functionally related to differencesin feedinghabits. Loxops,Himatione,
and apparentlyalsoPalmeria and Vestiaria feed by movingrapidly through
the foliage and gleaning insects from exposedleaf and bark surfaces.
Psittirostraand Hemignathusare moresedentary,respectivelyeatingseeds
and probing forcefully into bark crevicesfor insects. For the latter behavior a stronger grip might well be advantageousin helping the bird
maintain its position on the branch. In a comprehensivestudy of the
hind limb musclesof the New World nine-primariedoscinesto be published
later, I have found this general relationship to hold true. For example,
the shank musclesof the insectivorousParulidae are generally lessrobust
than thoseof the closelyrelated seed-eatingEmberizine finches. Someof
this variation may be attributable to allometric changesin musclesize, as
the forms with larger musclesare generallyof slightly larger body size.
The lossof M. plantaris in a few forms (Table 1) is of unknown significance. This tiny muscleis not infrequently lost in passerines.Gaunt
(1969) found that it is absent in most Hirundinidae, and I have found
a tendencyfor its loss in other groups,especiallythe Cardueline finches.
The tibial head of M. peroneusbrevis,presentin all forms studied,
has not been describedin birds before. The generaluniformity of the
pelvic myology,includingthe conditionof M. peroneusbrevis,strongly
supports the belief that the Depanididaeare a monophyleticgroup
descendedfrom a singlecommonancestor.The similarity of ttimatione,
October 1976]
Hawaiian HoneycreeperMyology
791
Palmeria, and Vestiaria (subfamily Drepanidinae) to the other forms
studied(subfamilyPsittirostrinae)furtherarguesthat thesetwo divisions
of the familyaroseby an early splittingof a singleancestralgrouprather
than from two differentfoundingspecies.Finally, the hind limb myology
of the Drepanididae
confirmsthat this familyis correctlyplacedwithin
the New World nine-primariedoscineassemblage,
and that its closest
relativesare amongthe fringillid subfamilyCarduelinae.A full account
of the basisof theseconclusions
will be presentedlater.
ACKNOWLEDG1VtENTS
I am grateful to the followingpersonsfor makingspecimens
availablefor dissection:
A. J. Berger,University of Hawaii, Honolulu; R. L. Zusi, National Museum of Natural
History, WashingtonD.C.; A. C. Ziegler,BerniceP. BishopMuseum,Honolulu; and
P. J. K. Burton, British Museum (Natural History), Tring. The drawings were
made by Lee Ambrose. This study was supportedby N.I.H. grant No. 1-F02-GM-36,
212~01 and N.S.F. grant No. BMS74-18079.
SUMMARY
The hind limb myologyof the Hawaiianhoneycreepers
(Drepanididae)
is describedin detail. In the 11 formsin 10 speciesand 7 generastudied,
little variationoccurs,attestingto the unity of this insular family. The
spectacular
adaptiveradiationin the feedingapparatusof the Drepanididae
is not reflectedto any great extentin the hind limb musculature.
LITERATURE
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W. B. 1954. Myology and serology of the avian family Fringillidae, a
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Department of Life Sciences,University of Pittsburgh, Pittsburgh,
Pennsylvania15260. Accepted2 May 1975.