Previous studies of hindlimb muscles suggest that reduction and individual variation in M. flexor cruris lateralis may be causally related to ecological habits such as aerial-foraging behavior. Examination of the muscle in a number of behaviorally convergent birds suggests that such variation is phylogenetically very restricted. Comparison with a published phylogeny of hindlimb muscle characters indicates that behavior and morphology have not coevolved in the case of M. flexor cruris lateralis. Examination of other hindlimb muscles suggests that individual variation is not likely to interfere with attempts to reconstruct phylogeny using such data. Received 3 October 1991, accepted 12 March 1992.
Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109, USA
IN AN EARLIER study (McKitrick 1985, 1986), I
dissected large series of numerous species of
tyrant flycatchers (Tyrannidae) and found
considerable individual variation in several
muscles of the hindlimb. In particular, M. flexor
cruris lateralis showed a trend toward size re-
duction and, in some cases, loss of the accessory
portion (pars accessoria) of the muscle (see
McKitrick 1986:fig. 1). The function of the pel-
vic part of the muscle (pars pelvica) is to flex
the shank (tibiotarsus), while pars accessoria ex-
tends the thigh (femur; Raikow 1985). The sig-
nificance of individual variation in size of this
muscle is unknown, but three hypotheses have
been proposed (McKitrick 1986). (1) Adapta-
tive-variation hypothesis: individuals with dif-
ferent morphologies forage in different ways,
thereby dividing the resource spectrum and
avoiding intraspecific competition. (2) Trans-
formation hypothesis: the variation is transient
and represents a temporary stage in the process
of reduction and eventual loss of the accessory
portion of M. flexor cruris lateralis. (3) Random-
variation hypothesis: the morphology of the
muscle is more or less irrelevant to aerially for-
aging birds, and the muscle may vary at ran-
dom. Further work suggested that the variation
is heritable (McKitrick 1990a, b), indicating that
it is not entirely due to nongenetic develop-
mental phenomena. However, marked left-right
asymmetry in muscle size (McKitrick 1990b)
hints that size is not under strong selective con-
trol, and preservation of variation by natural
selection (hypothesis 1) is probably not occur-
ring.
A few other hindlimb muscles showed qual-
itative individual variation of a lesser magni-
tude. M. iliotibialis lateralis varied in whether
a strap-shaped remnant of pars postacetabularis
was present. M. flexor hallucis longus varied in
the presence and number (0-2) of intermediate
heads. A quantitative variant of M. flexor dig-
itorum longus also was striking: in some spec-
imens the femoral head was very large, while
in others it was tiny (McKitrick 1985).
I undertook this study for three reasons. The
first was to determine the influence of phylog-
eny and ecology on individual variation in M.
flexor cruris lateralis. Few studies of individual
variation in avian limb musculature have been
reported, but Berman et al. (1990) and Raikow
et al. (1990) suggested that variation of the ex-
tent found by McKitrick (1986) may be uncom-
mon in birds (i.e. the variation may be peculiar
to tyrant flycatchers and, thus, simply a phy-
logenetic phenomenon).
Alternatively, the variation may be related to
ecology. For example, a robust thigh extensor
may be unnecessary in an aerial-foraging bird
and may be lost over the course of evolutionary
time, or at least released from constraint. In this
case, "rules" for the evolution of the hindlimb
musculature would apply to all species, regard-
less of phylogeny, and variation may conform
to one of the hypotheses suggested by Mc-
Kitrick (1986).
Finally, the variation could be related to both
phylogeny and ecology (i.e. the variation is re-
lated to habit, but for some reason has only
occurred in New World flycatchers). If this is
the case, then the hypotheses set forward by
McKitrick (1986) would apply only to tyrant
flycatchers. To try to address these problems, I
dissected representatives of a number of groups
of birds whose aerial-foraging behavior is prob-
ably of independent origin, so as to determine
whether similar patterns of individual variation
will occur in species that have kingbirdlike ae-
rial-foraging behavior.
A second component of this research address-
es the question of the relationship between the
origin of aerial-foraging behavior and the re-
duction of M. flexor cruris lateralis (FCL) among
species. A preliminary survey within the Tyran-
nidae (McKitrick 1985, 1986) showed that the
tyrannids with the most aerial foraging-habits
(e.g. Tyrannus, Sayornis, Contopus, Hirundinea)
have the most reduced FCL, whereas those with
the most terrestrial habits (e.g. Machetornis) have
the most robust FCL. From these observations,
I hypothesized that the association between ae-
rial-foraging behavior and muscle reduction is
a causal one. If this hypothesis is correct, the
association will be found in all birds showing
the same behavior as these tyrant flycatchers.
To test this prediction, I map the occurrence of
kingbirdlike foraging behavior onto a phylog-
eny of birds based on hindlimb-muscle mor-
phology (McKitrick 1991) in order to examine
the relationship between the evolution of ae-
rial-foraging behavior and the evolution of FCL
within a historical context. Finally, I wished to
examine variation in all the other hindlimb
muscles and attempt to evaluate the conclusions
of Raikow et al. (1990) that intraspecific varia-
tion in avian hindlimb musculature usually will
not interfere with phylogenetic analysis.
(2); Artamidae, Artamus leucorhynchus (2); Dicruridae,
Dicrurus hottentottus (2); Hirundinidae, Hirundo rustica
(7, only FCL examined in 3 of these). The muscicapid
Terpsiphone mutata (8) was used as a behavioral "out-
group" or control; this is an insectivorous species that
is not highly aerial in its habits. The observations of
Passer domesticus by Berman et al. (1990) and of Hy-
locichla mustelina and Cardinalis cardinalis by Raikow et
al. (1990) serve as additional controls.
Methods of dissection are as described in McKitrick
(1985). Specimens are referred to by their museum
catalogue numbers with no preceding acronym; a list
of the specimens dissected and the institutions from
which they were borrowed is given in the Appendix.
Dissections were unilateral due to restrictions by some
lending institutions. Muscles were compared with
those of Tyrannus melancholicus (McKitrick 1985). I not-
ed where the muscles differed from the arrangement
in that species; otherwise, the description was limited
to "As in T. melancholicus" (for data tabulation on this
species, see McKitrick 1991). Where no intraspecific
variation is noted, all specimens of a given species
had the same morphology.
For the phylogenetic analysis, transitions in FCL
were examined using the results of McKitrick's (1991)
phylogenetic analysis of hindlimb musculature. The
latter analysis yielded 6,000 trees; a 75% majority-
rule consensus tree revealed that of 80 groupings in
that tree, 65 occurred in all 6,000 trees. The remaining
15 were present in 79% or more of all trees. In other
words, the 6,000 trees were very similar in general
pattern; one of these (tree 1) was selected for exam-
ination of the general pattern of evolutionary tran-
sitions in FCL.
METHODS
Species were chosen for study on the basis of their
aerial feeding habits. Species were sought that typi-
cally forage for flying insects in a kingbirdlike man-
ner: scanning the area from a stationary perch, sal-
lying forth to capture the insect on the wing, and
then perching again to consume the prey. Such spe-
cies include bee-eaters (Meropidae; Fry 1972, pers.
observ.), rollers (Coraciidae; Clancey 1964, Frith 1979),
jacamars (Galbulidae; Fry 1970, Wetmore 1968), wood-
swallows (Artamidae; Frith 1979), and drongos (Di-
cruridae; Clancey 1964, Frith 1979, Keast 1972). I also
selected three highly aerial species that forage for
extended periods without perching between cap-
tures: a nighthawk (Caprimulgidae), a swift (Apodi-
dae), and a swallow (Hirundinidae). This selection
well represents the diversity in aerial-foraging be-
havior among birds.
Individuals of the following species were dissected
(number of specimens indicated in parentheses): Cap-
rimulgidae, Chordeiles minor (4); Apodidae, Chaetura
pelagica (8); Meropidae, Merops albicollis (5), M. viridis
(5, FCL only), M. apiaster (5, FCL only); Coraciidae,
Eurystomus orientalis (2); Galbulidae, Galbula ruficauda
RESULTS
Muscle descriptions are included below. The mus-
cle is listed and then variants are detailed.
M. ILIOTIBIALIS CRANIALIS (ICR)
Merops albicollis, Eurystomus orientalis, Chordeiles mi-
nor, Galbula ruficauda, Dicrurus hottentottus, Artamus leu-
corhynchus, and Terpsiphone mutata.--All specimens as
in T. melancholicus.
Chaetura pelagica.--As in T. melancholicus, but origin
relatively broad (about 5 mm); passes over distal por-
tion of M. scapulohumeralis caudalis. Insertion by
semitendinous fibers on head of tibiotarsus. Gap of
1-3 mm occurs along lateral edge of M. iliotrochan-
tericus caudalis between ICR and IL.
Hirundo rustica.--As in T. melancholicus, but varies
in width at origin. Width is 5.87 mm in 2487, 6.34
mm in 2642, 7.11 mm in 3501, and 4.89 in 226,783.
M. ILIOTIBIALIS LATERALIS (IL)
Merops albicollis, Eurystomus orientalis, Chaetura pe-
lagica, and Hirundo rustica.--As in T. melancholicus; only
pars preacetabularis present.
Chordeiles minor.--Pars postacetabularis well devel-
oped, extending entire length of dorsolateral lilac crest.
Pars acetabularis present, pars preacetabularis apo-
neurotic.
Galbula ruficauda.--Entire muscle absent.
Dicrurus hottentottus.--Pars preacetabularis and a
very narrow postacetabularis present.
Artamus leucorhynchus.--Pars acetabularis and pre-
acetabularis present; pars postacetabularis very slight.
Terpsiphone mutata.--All three parts present in most
specimens. Pars postacetabularis absent in 345928.
M. ILIOFIBULARIS (IF)
Merops albicollis, Eurgstomus orientalis, Chordeiles mi-
nor, Galbula ruficauda, Dicrurus hottentottus, Artamus leu-
corhgnchus, Terpsiphone mutata, and Hitundo rustica.--
As in T. melancholicus.
Chaetura pelagica.--As in T. melancholicus. A tendi-
nous "string" runs from distal one-fourth of IF's lat-
eral surface, down to GL and along latter's surface to
its origin. Beddard (1898) found such a string in Stru-
thio, Anatidae, some Rallidae, and some Alcidae.
M. ILIOFF. MORAI. IS EXTERNIJS (IFE)
Merops albicollis, Eurystomus orientalis, Chaetura pe-
lagica, Galbula ruficauda, Artamus leucorhynchus, Hirundo
rustica, and Terpsiphone mutata.--Absent.
Chordeiles minor.--Present in 506049, in which it is
2.04 mm wide distally and 2.5 mm long. Fibers ori-
ented in different direction from ITCA. In other three
specimens, it is difficult to determine whether muscle
is actually present and independent, or fused with
ITCA.
Dicrurus hottentottus.--Absent in 1971.3.5, but pres-
ent in 1940.12.8.348 and as described by Raikow et
al. (1979) for bowerbirds.
M. ILIOTROCHANTERICUS CAUDALIS (ITCA),
M. ILIOTROCHANTERICUS CRANIALIS (ITCR),
M. ILIOFEMORALIS INTERNUS (IFI),
g. FEMOROTIBIALIS MIDIUS (FTM),
M. FEMOROTIBIALIS INTERNUS (FtI),
M. CAUDOFEMORALIS (CF),
M. ISCHIOFEMORALIS (ISF)
All specimens as in T. melancholicus.
M. ILIOTROCHANTERICUS MEDIUS (ITM)
Chaetura pelagica.--Absent.
All other specimens as in T. melancholicus.
M. FEMOROTIBIALIS EXTERNUS (FTE)
Merops albicollis, Eurystomus orientalis, Artamus leu-
corhynchus, Chordeiles minor, Galbula ruficauda and Terp-
siphone mutata.--As in T. melancholicus.
Chaetura pelagica.--Lacks pars distalis.
Dicrurus hottentottus.--In 1940.12.8.348 pars distalis,
if present, not separable from pars proximaIls.
Hirundo rustica.--Pars distalis not discernible in
226,783.
M. FLEXOR CRURIS LATERALIS (FCL)
Merops albicollis.--121,166 (Fig. lc), only pars pel-
vica (FCLP) present. For 121,170, a small pars acces-
sofia (FCLA) present in addition to FCLP (Fig. la).
Muscle in this specimen most closely resembles vari-
ant 6a of McKitrick (1986:fig. 1), except insertion of
FCLA is limited to intercondylar region of the femur;
no fibers insert on lateral surface of the femoral shaft.
In 121,171 (Fig. lb) and 121,174, tendon G of FCLA
present but lacking fibers. In 121,179, muscle as in
121,170 except FCLA smaller, barely separable from
GI; tendons G and M are back to back.
Merops viridis.--Tendon G of FCLA present but
lacking fibers in 61293, 61313, and 61324. Tendon G
and FCLA both absent in 61297. A few distal fibers
remain of FCLA (as in some M. albicollis, M. apiaster,
and Hirundo rustica, see below) in 61310.
Merops apiaster.--Tendon G and small FCLA pres-
ent in 538004, 540150 and 540153, as in some speci-
mens of M. albicollis and one of M. viridis. Tendon G
present but fibers absent in 539921 and 540148.
Eurystomus orientalis.--FCLA present. In 1925.11.1.85,
FCLA robust, but insertion entirely intercondylar; no
fibers insert on shaft of femur. In 1925.11.1.87, FCLA
has a 3.47 mm insertion on femoral shaft. Origin of
FCLA's fibers entirely from tendon G; none from sur-
face of FCLP.
Chordeiles minor.--FCLA present and robust (Fig.
ld). Insertion on shaft of femur is 1.40 mm in 506049,
and 0.84 mm in 506050. In 506055 insertion on fem-
oral shaft limited to epicondyle and intercondylar
region; in 506056, it is entirely intercondylar. Tendon
G not exposed. FCLP has separate tendon from that
of FCM, but the two insert in common.
Chaetura pelagica.--George and Berger (1966) re-
ported that FCL is absent in swifts. More likely that
FCLP failed to separate from FCM. Origin of com-
bined muscle in these eight specimens extends over
entire area where the two muscles originate in other
birds (Fig. lel, le2). Very broad muscle with strong
tendinous insertion on tibiotarsus. No FCLA. No sign
of demarcation in large combined muscle in 039842,
but in other seven specimens demarcation evident on
medial surface, with caudal half of belly inserting
about 4 mm farther distad onto tendon of insertion
than cranial fibers.
Galbula ruficauda.--FCLA robust, but fibers do not
extend all the way down tendon G to GI, such that a
gap occurs on tendon G distally. Tendon M separated
from tendon of FCM until level of PL, at which point
the two tendons fuse and insert together on tibiotar-
SUS.
Dicrurus hottentottus.--FCLP stout (4.66 mm in
GI
'"'' FCRLP
RM
FCRLA
d
e(2)
PIF --
FCRLA
GI
FCRLA
FCRLP
?FCRM
GI
f g
Fig. 1. Variation in M. flexor cruris lateralis in selected specimens: (a) Merops albicollis, RGMT 121170; (b)
Merops albicollis, RGMT 121171; (c) Merops albicollis, RGMT 121166; (d) Chordeiles minor, USNM 506049; (el)
Chaetura pelagica, KU 039866 lateral view; (e2) with FDL removed; (f) Hirundo rustica, UMMZ 226914; (g) Hirundo
rustica, UMMZ 226783.
A/1971.3.5; 3.6 mm in 1940.12.8.348), but FCLA ab-
sent.
Artamus leucorhynchus.--FCLA present; insertion on
fernoral shaft 0.43 mm in A/1969.15.420 (femur 18.76)
and 0.40 mm in A/1969.15.421 (femur 18.3 mm). Ten-
don G not exposed. This morphology not exactly like
any represented in McKitrick (1986: fig. 1); the raphe
is as in fig. 1 (variant 2) but with narrow insertion.
Hirundo rustica.--Tendon G present in 2487, 2642,
3501, 225,913, 225,914, 226,243, and 226,783 with some
fibers on lateral surface of GI that could be remainder
of FCLA or part of G! (Fig. lf). Insertion of FCLA
entirely intercondylar. In 226,783 some fibers arise
proximal to ambiguous ones and insert on surface of
PIF (Fig. lg). See descriptions for Merops, above.
Terpsiphone mutata.--FCLA present and large; slight
gap between FCLA and GI occurs in 345895, but not
in other seven specimens.
M. FLEXOR CRURIS MEDIALIS (FCM)
Chaetura pelagica.--See description of FCL. All other
specimens as in T. melancholicus.
M. ILIOFEMORALIS (ILF)
Merops albicollis, Eurystomus orientalis, Chordeiles mi-
nor, Chaetura pelagica, Galbula ruficauda, Dicrurus hot-
tentottus, Hirundo rustica, and Terpsiphone mutata.--Ab-
sent.
Artamus leucorhynchus.--Present in A.1969.15.420;
absent in A.1969.15.421. Arises by tendinous fibers
on dorsolateral iliac crest, caudal to ilioischiadic fo-
ramen. Strap-shaped belly narrows to slender tendon
that inserts two-fifths of way down fernoral shaft, just
proximal to insertion of CF.
M. OBTURATORIUS LATERALIS (OL)
Merops albicollis.--Appears to have three heads of
roughly equal size in 121,166, although two lower
heads might be considered one. Dorsal (OLD) and
intermediate heads divided by tendon of OM. Two
heads present in 121,170, 121,171 and 121,174; dorsal
head bisected by tendon of OM. Two heads present
of equal size in 121,179: tendon of OM bisects OLD.
Eurystomus orientalis and Galbula ruficauda.--Pars
dorsalis present and small (in terminology of Raikow
1978).
Chordeiles minor.--OLD present and small in 506049,
small to medium in 506056, medium in 506050 and
506055.
Chaetura pelagica and Hirundo rustica.--OLD absent.
Dicrurus hottentottus.--OLD medium in 1971.3.5,
medium to large in 1940.12.8.348.
Artamus leucorhynchus.--OLD medium.
Terpsiphone mutata.--345895 and 345910, OLD me-
dium. In 345918, as 345895 except OLD is medium to
large. In 345916, OLD small; OLD and OLV equal in
length and OLD is one-half width of OLV. In 345921,
OLD medium to large; OLD slightly longer than OLV,
and the two are equal width. For 345924, 345928 and
345927, as in 345921 except OLD medium.
M. OBTURATORIUS MEDIALIS (OM)
Merops albicollis, Eurystomus orientalis, Chordeiles mi-
nor, Chaetura pelagica, Galbula ruficauda, Artamus leu-
corhynchus, Hirundo rustica, and Terpsiphone mutata.--
As in T. melancholicus.
Dicrurus hottentottus.--As in T. melancholicus, but has
two tendons of insertion that merge to insert as one.
M. PUBO-ISCHIO-FEMORALIS (PIF)
Merops albicollis and Eurystomus orientalis.--As in
Tyrannus melancholicus, except divided into deep and
superficial parts, not cranial and caudal parts.
Choralelies minor.--Clearly divided into deep and
superficial parts in all except 506055, in which no
separation evident.
Chaetura pelagica.--One undivided muscle mass
present.
Galbula ruficauda.--The two bellies of PIF fused dis-
tally on lateral surface of muscle in 1932.2.3.1, but
not in 1932.2.3.2. On medial surface there is complete
fusion.
Dicrurus hottentottus, Artamus leucorhynchus, Hirundo
rustica, and Terpsiphone mutata.--As in T. melancholicus.
M. AMBIENS (AM)
Absent in all specimens.
M. GASTROCNEMIUS, PARS LATERALIS (GL)
All specimens as in T. melancholicus.
M. GASTROCNEMIUS, PARS INTERMEDIA (GI)
For all specimens except Chaetura pelagica, as in T.
melancholicus.
Chaetura pelagica.--Muscle appears to have two heads
of origin, but this may represent fusion of PL with
GI. One head arises fleshy on proximal one-fourth of
caudal surface of fernoral shaft, and other arises on
medial condyle of femur. Combined muscle passes
half-way down tibiotarsus. PL arises on tibiotarsus,
not femur, in birds; present case could represent shift
in attachment of muscle mass.
M. GASTROCNEMIUS, PARS MEDIALIS (GM)
Merops albicollis.--Two heads of origin; medial one
as in T. melancholicus; lateral one arises on head of
tibiotarsus and passes lateral to insertion of FCL and
FCM. Lateral head appears to "replace" PL; alterna-
tively, it is PL and has fused with GM. The two heads
fuse about one-third way down tibiotarsus. No pa-
teliar band.
Chaetura pelagica, Eurystomus oriehtalis, and Galbula
ruficauda.--As in T. melancholicus. No deep head, and
no pateliar band.
Chordeiles minor and Dicrurus hottentottus.--Deep and
superficial heads and pateliar band present.
Artamus leucorhynchus and Hirundo rustica.--As in T.
melancholicus, and divided into deep and superficial
heads. No pateliar band.
Terpsiphone mutata.--Divided into deep and super-
ficial heads. A 0.60-mm pateIlar band present (see
Raikow 1978:18). No pateliar band in 345918.
M. PLANTARIS (PL)
Merops albicollis.--Maurer and Raikow (1981) re-
ported this absent in bee-eaters, but see description
under GM.
Eurystomus orientalis, Chordeiles minor, Galbula ruff-
cauda, Dicrurus hottentottus, Artamus leucorhynchus, and
Terpsiphone mutata.--As in T. melancholicus.
Chaetura pelagica.--Reportedly absent (George and
Berger 1966), but see description of GI.
Hirundo rustica.--Absent.
M. FLEXOR PERFORANS ET PERFORATUS
DIGITI II (FPPD2)
Merops albicollis.--Belly very small, arising by sem-
itendinous fibers and a short tendon from proximo-
caudal surface of lateral fernoral condyle. Bipinnate
belly passes one-fourth tibiotarsus before giving rise
to a slender tendon. Belly does not conceal FPPD3.
Eurystomus orientalis, Chaetura pelagica, Artamus leu-
corhynchus, and Terpsiphone mutata.--As in T. melan-
cholicus.
Chordeiles minor.--Tendon splits and inserts on ei-
ther side of base of phalanx 2, digit II.
Galbula ruficauda.--When tendon enters pes, it per-
forates tendon of FPD2 (contra Swierczewski and Rai-
kow 1981) and bifurcates, thus allowing passage of
FHL. Two branches insert on lateral and medial sides
of base of phalanx 2, digit II.
Dicrurus hottentottus.--At level of first phalanx of
digit II tendon is perforated, thus allowing passage
of tendon of FDL.
Hirundo rustica.--As in T. melancholicus, but inserts
on medial and lateral corners of base of phalanx 2,
digit II.
M. FLEXOR PERFORANS ET PERFORATUS
DIGITI III (FPPD3)
half-way down tibiotarsus and gives rise to flat ten-
don. Tendon perforated by FDL, and two resulting
branches insert on either side of phalanx 3 of digit
III. There are no vincula other than one securing ten-
don to phalanx. In 121,179, insertion on distal end of
lateral surface of phalanx 2, and at base of phalanx 3.
Eurystomus orientalis, Chaetura pelagica, Dicrurus hot-
tentottus, Artamus leucorhynchus, Hirundo rustica, and
Terpsiphone mutata.--As in T. melancholicus.
Chordeiles minor.--Inserts on either side of base of
phalanx 3, digit III, except in 506049, which is missing
third and ungual phalanx; tendon therefore stops at
phalanx 2.
Galbula ruficauda.--Unipinnate but approaching a
parallel-fibered condition. Single head arises from lat-
eral cnemial crest of tibiotarsus and from pateliar lig-
ament by tendinous fibers. Tendon of insertion passes
through lateral side of tibial cartilage and down plan-
tar surface of tarsometatarsus. Perforates tendon of
FPD3, and bifurcates, thus permitting passage of FDL;
the two branches insert on lateral and medial sides
of base of phalanx 3, digit III.
M. FLEXOR PERFORATUS DIGITI II (FPD2)
Merops albicollis.--Arises by aponeurotic sheet on
medial surface of FPD3, emerging as belly about half-
way down FPD3 and passing nearly length of tibio-
tarsus before becoming entirely tendinous. Tendon
inserts on base of phalanx 1, digit II.
Eurystomus orientalis.--Arises fleshy from deep sur-
face of tendon of origin of medial head of FPD3.
Fibers arise nearly one-fourth way down tibiotarsus,
and pass nearly length of that bone. Tendon of in-
sertion ensheathes that of FPPD2 at distal end of tar-
sometatarsus.
Chordeiles minor.--Situated on caudal surface of
shank, and arises tendinously from lateral condyle of
femur and from intercondylar region.
Chaetura pelagica.--Absent.
Galbula ruficauda.--In 1932.2.3.1, very slender, aris-
ing by tendon from intercondylar region of femur.
Branch of this tendon passes to deep surface of FPD3
and might be said to be a second origin of that muscle.
In 1932.2.3.2, as above, except there is an unknown
muscle arising in common with FPD2, from same ten-
don. That muscle is unipinnate, with fleshy belly aris-
ing one-third way down tibiotarsus and passing near-
ly length of that bone. Tendon passes through center
of tibial cartilage and inserts onto tendon of insertion
of FPD3 near proximal end of tarsometatarsus, as FL
would do if present.
Dicrurus hottentottus, Artamus leucorhynchus, Hirundo
rustica, and Terpsiphone mutata.--As in T. melancholicus.
Merops albicollis.--Cranial fibers arise by tendon on
later, al cnemial crest of tibiotarsus and from deep sur-
face of pateliar ligament; caudal fibers arise from deep
surface of pateIlar ligament and lateral condyle of
femur. Muscle is irregularly bipinnate. Belly passes
M. FLEXOR PERFORATUS DIGITI III (FDP3)
Merops albicollis.--Arises by semitendinous and
fleshy fibers from lateral condyle of femur in common
with FPD4 and FPD2.
Eurystomus orientalis.--Has two heads of origin and
lies deep to FPD4. Lateral head arises in common with
that of distal head of FPD4. Medial head of FPD3
arises by its own tendon in intercondylar region of
femur. Group of fleshy fibers arises from medial bor-
der of this tendon less than one-fourth way down
tibiotarsus. The two heads join one-fourth way down
that bone. In its proximal half, all fibers on lateral
side of muscle are on deep surface of common tendon
formed by fusion of the two heads. In distal half,
fibers arise on superficial surface of muscle as well.
Belly extends nearly length of tibiotarsus. Tendon
bifurcates, thus allowing passage of tendon of FDL,
and insertion is on lateral and medial sides of base
of phalanx 2, digit III.
Chordeiles minor.--Large muscle arising in intercon-
dylar region by fleshy and semitendinous fibers. There
is also a tendinous connection with tendon of lateral
head of FPD4, so muscle can be said to have two heads
of origin. Belly extends nearly length of tibiotarsus.
Chaetura pelagica.--As in Merops.
Galbula ruficauda.--Arises in intercondylar region.
A vinculum lies between FPD3 and FPPD3.
Dicrurus hottentottus.--As in T. melancholicus. FPD3
and FPD4 closely associated on their medial surface
due to aponeurosis on that surface. Both muscles sit-
uated on medial surface of shank.
Artamus leucorhynchus.--As in T. melancholicus. A
tendinous slip joins tendons of FPD3 and FPD4 about
two-thirds way down tarsometatarsus.
Hirundo rustica and Terpsiphone mutata.--As in T.
melancholicus.
M. FLEXOR PERFORATUS DIGITI ][V (FPD4)
Merops albicollis.--FPD4, FPD3, FPD2, and FHL all
closely associated. FPD4 arises by tendinous fibers
from lateral condyle of femur. Unipinnate belly ex-
tends two-thirds tibiotarsus; tendon arises from apo-
neurosis on surface of distal third of belly. Slender
tendinous branch attaches tendons of FPD4 and FPD3.
Tendon of insertion attaches at base of 2nd and 4th
phalanges, digit IV.
Eurystomus orientalis.--Arises by two heads: a small,
distal head by slender tendon from lateral condyle of
femur; and a larger, proximal head by flat tendon
from intercondylar region of femur. Belly of distal
head arises nearly one-fourth way down tibiotarsus.
The two heads join nearly immediately one-fourth
way down that bone to form common belly that ex-
tends about three-fifths that bone. Insertion on lateral
side of base of phalanx 2 and either side of phalanx
3, and at base of ungual phalanx, digit IV.
Chordeiles minor.--After removal of FPPD2 and
FPPD3, this is most superficial muscle remaining on
lateral surface of shank. Arises by two heads: tiny
lateral head arising by tendon on lateral condyle, and
larger medial head arising in intercondylar region.
Lateral belly fuses with medial belly after about 2
mm. Tendon of insertion splits to allow passage of
FDL, sending a medial branch to insert at base of
phalanx 2 and phalanx 3, and a lateral branch that
inserts on same phalanges. In 506050, only first pha-
lanx of digit IV present; muscle inserts by tendinous
fibers on joint capsule between tibiotarsus and tar-
sometatarsus. Tendon of FDL passes among these fi-
bers.
Chaetura pelagica.--Laterally situated, one head of
origin. Tendon of origin about 6 mm long.
Galbula ruficauda.--Single belly arises fleshy in in-
tercondylar region of femur. Closely associated on
medial surface with belly of FPD3, with which it aris-
es. Tendon does not bifurcate to allow passage of FHL.
Single insertion is broad on plantar surface of base
of phalanx 2, digit IV.
Dicrurus hottentottus, Hirundo rustica, and Terpsiphone
mutata.--As in T. melancholicus, but lack distal head.
Artamus leucorhynchus.--As in T. melancholicus.
M. FLEXOR HALLUCIS LONGUS (FHL)
Merops albicollis.--Single head of origin arises by
semitendinous fibers in close association with FPD2,
FPD3, and FPD4 in intercondylar region of femur.
Belly passes about seven-eighths tibiotarsus before
giving rise to tendon of insertion. Tendon fuses with
that of FDL, and common tendon gives rise to three
distal branches that insert on digits II-IV. A medial
branch emerging proximal to others inserts on digit I.
Eurystomus on'entalis.--Has two heads of origin: large
lateral head arising fleshy from lateral condyle and
lateral portion of intercondylar region of femur (it
appears very much like the large femoral head of FDL
that occurs in some tyrant flycatchers); and medial
head from intercondylar region deep to lateral head.
The two heads fuse less than one-fourth way down
tibiotarsus. Tendon of insertion joins lateral side of
that of FDL about one-third way down tarsometatar-
SUS.
Chordeiles minor.--Arises by one head, an extensive,
fleshy origin in intercondylar region and on lateral
epicondyle of femur. Has no tendinous origin from
lateral condyle. Belly extends two-fifths of tibiotarsus.
Tendon fuses with that of FDL in proximal one-fourth
of tarsometatarsus.
Chaetura pelagica.--Arises by two heads: lateral or
fibular head from dorsal surface of head and shaft of
fibula; medial or tibial head arises on second fifth of
dorsal surface of tibiotarsus. The two heads fuse one-
third way down tibiotarsus. Tendon of insertion fuses
with that of FDL as described below.
Galbula ruficauda.--Arises by three heads: lateral head
from head of fibula; intermediate one from lateral
condyle of femur; and medial one from intercondylar
region of femur. The three merge less than one-fourth
way down tibiotarsus. Tendon inserts on ungual pha-
lanx of digits I, II and IV.
Dicrurus hottentottus.--Enormous muscle, largest of
hindlimb. Medial head arises by semitendinous fibers
independently of FPD3 and FPD4. The three bellies
fuse about two-fifths way down tibiotarsus to form
common belly, which extends length of latter bone.
Tendon of FHB does not appear to ensheathe that of
FHL.
Artamus leucorhynchus.--As in T. melancholicus, ex-
cept tendon of FHB does not appear to ensheathe that
of FHL.
Hirundo rustica.--Three heads of origin: tiny lateral
head arises by tendon in common with that of FPD2,
and belly itself arises one-fourth way down tibiotar-
sus. Large medial head arises as in T. melancholicus;
tiny intermediate head arises by slender tendon in
common with medial head and passes medial to ten-
don of IF. Some specimens of T. melancholicus are sim-
ilar.
Terpsiphone mutata.--Muscle most closely resembles
figure 16b in McKitrick (1985), except lateral head is
quite small, and intermediate head is three to four
times size of lateral head. The three heads fuse about
one-fourth way down tibiotarsus. Insertion as in T.
melancholicus.
M. FLEXOR DIGITORUM LONGUS (FDL)
Merops albicollis.--Most deeply situated muscle on
shank. Has fibular and tibial head of origin. Fibular
head arises medial to tendon of IF. See description of
insertion under FHL (above). Where tendon of FDL
trifurcates is a small bundle of muscle fibers; may be
M. lumbricalis.
Eurystomus orientalis.--Two heads of origin. Fibular
and tibial heads as in T. melancholicus. Two heads fuse
less than one-fourth way down tibiotarsus. Insertion
includes elastic bands at: distal end of phalanx 1, digit
I; distal end of phalanx 2, digit II; base of phalanx 3
and distal end of phalanx 3 in digit III; and base of
phalanx 4 and distal end of phalanx 4, digit IV.
Chordeiles minor.--No femoral head. Muscle extends
nearly the length of tibiotarsus and inserts on ungual
phalanx (where present) of each digit. Elastic band
occurs at each phalanx. In 506050, which lacks most
of digit IV, FDL sends no branch to digit IV.
Chaetura pelagica.--Extremely large, arising on dis-
tal half of femoral shaft; belly extends two-fifths way
down tibiotarsus and gives rise to stout tendon. Ten-
don of FHL fuses with it after they emerge from tibial
cartilage. About three-fifths way down tarsometatar-
sus, a branch to hallux arises and inserts on base of
its ungual phalanx. Immediately distal to origin of
this branch, tendon of FDL trifurcates. Branches in-
sert on base of ungual phalanx on each of the three
digits.
Galbula ruficauda.--Arises fleshy on medial surface
of fibula about one-eighth way down tibiotarsus, and
from caudolateral and caudomedial surface of that
bone one-fourth way down. Belly passes length of
tibiotarsus. Insertion at base of ungual phalanx of
digit III.
Dicrurus hottentottus.--As in T. melancholicus. Fem-
oral head 2.54 mm deep in 1971.3.5, and 4.74 mm in
1940.12.8.348.
Artamus leucorhynchus.--As in T. melancholicus, ex-
cept no fernoral head in 1969.15.420.
Hirundo rustica.--Has small fibular head, moderate-
ly sized fernoral head, and a tibial head. Insertion as
in T. melancholicus.
Terpsiphone mutata.--as in T. melancholicus.
M. POPLITEUS (POP)
Merops albicollis, Chaetura pelagica, Dicrurus hotten-
tottus, Artamus leucorhynchus, Hirundo rustica, and Terp-
siphone mutata.--Absent.
Eurystomus orientalis, Chordeiles minor, and Galbula
ruficauda.--Small, parallel-fibered muscle arising on
medial surface of head of fibula; inserts on caudolater-
al surface of tibiotarsus.
M. FIBULARIS LONGUS (FL)
Merops albicollis and Chaetura pelagica.--Absent.
Eurystomus orientalis.--Arises on distal end of fibula.
Belly occupies only third quarter of tibiotarsus. In-
sertion as in T. melancholicus.
Chordeiles minor.--As in T. melancholicus. Has two
points of insertion, one on tibial cartilage and one on
tendon of FPD3.
Galbula ruficauda.--Absent, but see description for
FPD2.
Dicrurus hottentottus and Hirundo rustica.--As in T.
melancholicus, except tendon of insertion does not bi-
furcate, but simply attaches on proximolateral corner
of tibial cartilage.
Artamus leucorhynchus.--As in T. melancholicus.
Terpsiphone mutata.--Has aponeurotic attachment
on medial surface to medial surface of TCR. Aponeu-
rosis arises from pateliar crest. Some fibers from lat-
eral surface of FB attach to deep surface of FL. Tibial
head of TCR attaches firmly to tendinous sheet it
shares with FL, proximally. This sheet arises from
caudal surface of lateral cnemial crest.
M. FIBULARIS BREVIS (FB)
Merops albicollis.--As in T. melancholicus but arises
only on distal one-fourth fibula and not held in place
by retinaculum.
Chordeiles minor.--Absent.
Chaetura pelagica, Dicrurus hottentottus, Artamus leu-
corhynchus, and Terpsiphone mutata.--As in T. melan-
cholicus.
Galbula ruficauda.--Slender and bipinnate, arising
by semitendinous fibers on distal half of fibula. Passes
length of shank. Tendon arises as aponeurosis on dis-
tal half of muscle's surface. Inserts as in T. melan-
cholicus, but no retinaculum.
Hirundo rustica.--As in T. melancholicus, but no ret-
inaculum.
M. TIBIALIS CRANIALIS (TCR)
Merops albicollis.--As in T. melancholicus, except fern-
oral head smaller than tibial head, no "smaller ten-
don" by which fernoral head arises, and no bifurca-
tion of tendon of insertion.
Eurystomus orientalis, Chordeiles minor, Chaetura pe-
lagica, Galbula ruficauda, Artarnus leucorhynchus, Dicrurus
hottentottus, Hirundo rustica, and Terpsiphone mutata.--
As in T. melancholicus.
M. EXTENSOR DIGITORUM LONGUS (EDL)
Merops albicollis.--Arises fleshy from lateral surface
of cranial and cnemial crest, from Sulcus intercristalis,
and cranial surface of proximal half of tibiotarsus.
Belly extends three-fourths tibiotarsus. Tendon tri-
furcates two-thirds way down tarsometatarsus and
inserts on ungual phalanx of digits ll-lV. Branches
go through fibrous canal on dorsal surface of each
basal phalanx. Branch to digit Ill divides at distal end
of phalanx 2, inserting at base of phalanx 3 on cranio-
medial surface.
Eurystornus orientalis.--Origin from inner (caudal)
surface of cranial cnemial crest and from caudal sur-
face of tibiotarsus. Belly bipinnate nearly length of
that bone. Insertions as follows: digit ll with main
branch on base of ungual phalanx and short broad
branch on base of phalanx 2; digit lll with branch
attaching broadly to base of phalanges 2 and 3, and
distal to phalanx 3 it narrows and inserts on ungual
phalanx; digit IV with branch attaching broadly at
base of phalanges 2-4, narrows to insert on ungual
phalanx.
Chordeiles minor.--Bipinnate to over three-fourths
tibiotarsus. Insertion as follows: digit I1 with main
branch on base of ungual phalanx, and short (medial)
branch on base of phalanx 2; digit Ill with branch
inserting broadly at base of phalanx 2, then continues
to ungual phalanx (except in 506049, in which only
two phalanges present for digit lll); digit IV with one
branch to base of ungual phalanx (except in 506050,
in which branch passes to plantar surface of tarso-
metatarsus and attaches broadly at distal end, near
base of digit IV).
Chaetura pelagica.--Origin as in T. melancholicus. Bel-
ly extends nearly length of tibiotarsus and is bipin-
hate entire length. Insertion simpler than in T. me-
lancholicus, tendon trifurcates at distal end of
tarsometatarsus, and each branch inserts on ungual
phalanx of its respective digit.
Galbula ruficauda.--Arises fleshy from lateral surface
of cranial cnemial crest, and medial and lateral sur-
faces of lateral cnemial crest. Extends seven-eighths
tibiotarsus. Tendon of insertion sends branch to digits
ll, lll and IV. Branch to digit ll simply inserts on
dorsal surface of ungual phalanx. Branch to digit lll
inserts broadly on dorsal surface of 3rd phalanx, then
sends branch to dorsal surface of ungual phalanx.
Branch to digit IV inserts simply on ungual phalanx.
Dicrurus hottentottus.--For most specimens as in T.
melancholicus. In 1940.12.8.348 a retinaculum holds
tendon in place at distal end of tarsometatarsus, and
a retinaculum holds each of main branches in place
at proximal end of each of the three digits. Branch to
digit lll splits into four branches. More medial of two
inner branches inserts on dorsal surface of base of
phalanx 2. Medial and lateral branches insert together
on dorsal surface of base of ungual phaianx. More
lateral of two inner branches inserts on dorsal surface
of base of phalanx 3. Branch to digit IV inserts on
base of ungual phalanx, but sends short branch to
insert at base of phalanx 2, one to phalanx 3, and one
to phalanx 4. In 1971.3.5, on digit ll it is medial branch
that goes to ungual phalanx and lateral one to base
of digit. Branch to digit IV ends at base of phalanx 4
and no insertion on ungual phalanx, although an
elastic band occurs between 4th and ungual phalan-
ges.
Artamus leucorhynchus.--lnsertion as follows: on digit
I1, a tiny branch inserts at base of phalanx 2, while
main branch inserts at base of ungual phalanx; on
digit lll, main branch splits into three, with central
branch inserting at base of phalanx 2, and lateral and
medial branches inserting together at base of ungual
phalanx. Branch to digit IV bifurcates at base of pha-
lanx 3; medial branch goes to base of phalanx 4 and
lateral branch inserts at base of ungual phalanx.
Hirundo rustica.--Origin as in T. melancholicus. In-
sertion as follows: in digit ll, branch attaches broadly
at base of phalanx 2 and inserts on ungual phalanx;
in digit lll, branch bifurcates, with medial branch
attaching at base of phalanx 2, then sending another
branch to ungual phalanx, and lateral branch bifur-
cates distal to phalanx 1, with one part attaching at
base of phalanx 3, and the other at ungual phalanx;
in digit IV, a branch attaches medially to base of pha-
lanx 4, lateral branch to ungual phalanx.
Terpsiphone rnutata.--As in T. melancholicus, except
branch to digit ll inserts on ungual phalanx, with
lateral branch to phalanx 2. At digit lll, tendon
branches in distal two-thirds of phalanx 1. Medial
branch then bifurcates, and lateral part inserts at base
of phalanx 2, while medial part inserts at base of
ungual phalanx. Lateral branch bifurcates at base of
phalanx 2; medial part inserts at base of phalanx 3
and lateral part inserts at base of ungual phalanx.
M. FLEXOR HALLUCIS BREVIS (FHB)
Merops albicollis.--As in T. melancholicus, except with
double tendon of insertion. Tendon perforated by
FDL at base of hallux.
Eurystomus orientalis.--Robust, bipinnate muscle
arising on medial surface of hypotarsus and hypo-
tarsal ridge. Extends nearly length of tarsometatarsus.
Broad tendon of insertion ensheathes hallucal branch
of FDL, thereby forming two branches. These give
rise to tendinal "saddle" that inserts on lateral and
medial sides of base of phalanx 1 of hallux.
Chordeiles minor.--As in T. melancholicus, except ten-
don is double distally, and is not perforated by FHL.
Chaetura pelagica.--Arises fleshy on caudal surface
of medial cotyla of tarsometatarsus, and from medial
surface of hypotarsus. Bipinnate to half of tarsometa-
tarsus, and unipinnate to nearly length of that bone.
Inserts by flat tendon on base of phalanx 1 of hallux.
Belly covered proximally by aponeurosis arising on
medial condyle of tibiotarsus and inserting on medial
surface of tarsometatarsal shaft and caudal edge of
EHL.
Galbula ruficauda.--Small, arising on medial surface
of hypotarsus and from medial surface of hypotarsal
ridge. Insertion as in T. melancholicus.
Dicrurus hottentottus and Artamus leucorhynchus.--As
in T. melancholicus.
Hirundo rustica.--As in T. melancholicus, but no notch
evident.
Terpsiphone mutata.--As in T. melancholicus. Slight
notch in 345895, 345910, 345921 and 345924 but notch
absent from other four specimens.
M. ADDUCTOR DIGITI II (ADD2)
Merops albicollis.--Weak muscle extending one-half
length of tarsometatarsus, giving rise to slender ten-
don.
Eurystomus oentalis.--Flat, bipinnate muscle aris-
ing in Sulcus flexorius deep to tendon of FDL but not
connected with it in any way. Fibers pass two-thirds
length of tarsometatarsus. Robust tendon inserts at
base of digit II on lateroplantar surface.
Chordeiles minor and Chaetura pelagica.--Arises on
lateral cotyla of tarsometatarsus and on hypotarsus.
Extends length of tarsometatarsus, and narrows to
slender tendon that inserts on lateral surface of base
of phalanx 1.
Galbula ruficauda.--Arises just distal to, and on, lat-
eral and medial hypotarsal crests. Passes slightly more
than half tarsometatarsus. Insertion as in Chordeiles
and Chaetura.
Dicrurus hottentottus, Artamus leucorhynchus, Hirundo
rustica, and Terpsiphone mutata.--Absent.
M. EXTENSOR HALLUCIS LONGUS (EHL)
Merops albicollis.--Arises by one head extending
length of tarsometatarsus; inserts at base of ungual
phalanx of hallux.
Eurystomus orientalis.--As in T. melancholicus, but ro-
bust. No origin from Tuberositas M. tibialis cranialis.
Chordeiles minor.--As in T. melancholicus, but a pars
distalis present as illustrated in Hoff (1966: fig. 7 and
11 [muscle not labeled as such]).
Chaetura pelagica.--As in T. melancholicus, but no or-
igin from Tuberositas M. tibialis cranialis.
Galbula ruficauda.--Slender, arising by fleshy and
semitendinous fibers on craniomedial surface of me-
dial cotyla of tarsometatarsus. Belly passes length of
that bone, along dorsal (outer) surface of hallux; in-
serts at base of ungual phalanx.
Dicrurus hottentottus, Artamus leucorhynchus and Hi-
rundo rustica.--As in T. melancholicus.
Terpsiphone mutata.--As in T. melancholicus, but small
bundle of fibers arises on phalanx 1 of hallux and
inserts on distal end of tendon of insertion.
M. ABDUCTOR DIGITI II (ABD2)
Merops albicollis, Dicrurus hottentottus, Artamus leu-
corhynchus, Hirundo rustica, and Terpsiphone mutata.--
Absent.
Eurystomus orientalis.--Slender, bipinnate muscle
arising fleshy in distal half of dorsomedial surface of
tarsometatarsus. Inserts by short tendon on the ven-
tromedial corner of first phalanx of digit II.
Chordeiles minor.--Small, irregularly fan-shaped
muscle arising at distal end of dorsomedial surface of
tarsometatarsus. Insertion as in Eurystomus.
Chaetura pelagica.--As in Chordeiles.
Galbula ruficauda.--As in Eurystomus.
M. EXTENSOR PROPIHUS DIGITI III (EPD3)
Merops albicollis.--In 121,166, 121,171 and 121,174,
bipinnate. Extends length of cranial surface of tar-
sometatarsus and inserts on cranial surface of base of
phalanx 1. In 121,170 and 121,179, insertion double.
Tendon splits and the two branches insert on either
side of base of phalanx 1.
Eurystomus orientalis and Galbula ruficauda.--Arises
fleshy just distal to Tuberositas M. tibialis cranialis on
dorsal surface of tarsometatarsus. Some fibers also arise
on tendon of TCR near latter's insertion. Fibers arise
from tarsometatarsus for nearly length of that bone.
Insertion on dorsal surface of base of phalanx 1.
Chordeiles minor.--As in Eurystomus and Galbula, but
confined to distal half of tarsometatarsus.
Chaetura pelagica, Dicrurus hottentottus, Artamus leu-
corhynchus, Hirundo rustica, and Terpsiphone mutata.--
Absent.
M. ABDUCTOR DIGIT][ IV (ABD4)
Merops albicollis.--Narrow, unipinnate, lying on lat-
eral surface of tarsometatarsus; extends length of that
bone.
Eurystomus orientalis and Galbula ruficauda.--Arises
just distal to lateral cotyla of the tarsometatarsus in
Sulcus flexorius. Belly extends length of tarsometa-
tarsus; tendon passes through retinaculum before in-
serting on lateroplantar surface of phalanx 1.
Chordeiles minor.--Lies on caudolateral surface of
tarsometatarsus. Arises lateral to Sulcus flexorius one-
third way down tarsometatarsus, passes length of that
bone, and narrows to tendon. Inserts on lateral sur-
face of base of phalanx 1.
Chaetura pelagica.--As in Chordeiles, but arises one-
third to two-fifths way down tarsometatarsus.
Dicrurus hottentottus.--Tiny, irregularly strap-shaped
muscle arising fleshy on caudal surface of lateral
trochlea of tarsometatarsus. Has broad, tendinous in-
sertion on surface of ligament between tarsometatar-
sus and base of phalanx 1.
Artamus leucorhynchus.--Absent in 1969.15.420. In
1969.15.421 a few weak fibers found in this area, but
no well-defined muscle.
Hirundo rustica.--Absent.
Terpsiphone mutata.--Absent, although in 345918 and
345924 there appear to be a few fibers that could be
a vestigial ABD4.
M. EXTENSOR SREVIS DIGITI IV (EBD4)
Merops albicollis, Dicrurus hottentottus, Artamus leu-
corhynchus, Hirundo rustica, and Terpsiphone mutata.--
Absent.
Eurystomus orientalis.--Slender, bipinnate muscle
lying on dorsolateral surface of tarsometatarsus. Aris-
es fleshy the length of tarsometatarsus next to mystery
extensor of digit III (see below). Passes between toes
and appears to insert on plantar surface of base of
phalanx 1. Action would appear to be flexion rather
than extension.
Chordeiles minor and Chaetura pelagica.--Arises in
Sulcus extensorius on dorsal surface of tarsometatar-
sus. Passes length of that bone and narrows to tendon
that passes through canal in distal end of bone. Ten-
don inserts on medial surface of base of phalanx 1.
Galbula ruficauda.--Largest of intrinsic muscles of
pes, occupying entire dorsolateral surface of tarso-
metatarsus. Bipinnate and arises fleshy from nearly
entire length of tarsometatarsal shaft. Tendon inserts
at base of phalanx 1.
M. LUMBRICALIS (L)
Merops albicollis. -- See description under FDL
(above).
Eurystomus orientalis, Dicrurus hottentottus, Artamus
leucorhynchus, Hirundo rustica, and Terpsiphone muta-
ta.--Absent.
Chordeiles minor.--Present on deep surface of com-
mon tendon of FDL and FHL.
Chaetura pelagica.--A few fibers present on tendon
of insertion of FDL.
Galbula ruficauda.--A few fibers present on distal
end of tendon of FDL in 1932.2.3.2, but none in
1932.2.3.1.
UNIDENTIFIED MUSCLES
In Eurystomus orientalis, two extra intrinsic muscles
occur in foot. One, to digit II, arises fleshy just distal
to Tuberositas M. tibialis cranialis, next to EPD3. In-
serts by a very slender tendon at base of phalanx 1,
digit II on dorsolateral side. Present in 1925.11.1.85,
but not 1925.11.1.87. The second, to digit III, is present
in both specimens of Eurystomus. Narrow but well-
defined, bipinnate muscle arising on dorsal surface
of proximal end of tarsometatarsus. Passes length of
that bone and inserts by short tendon at base of pha-
lanx 1, digit III, on dorsolateral side.
In Chordeiles minor, a narrow, very distinct strap-
shaped muscle arises fleshy near tendon of EHL at
distal end of caudal surface of tarsometatarsus, prox-
imal to metatarsal I. Inserts by semitendinous fibers
on caudal surface of metatarsal I, with some fibers
inserting at base of phalanx I, digit I. Muscle was not
mentioned by Hoff (1966). Does not appear to be ho-
mologous with EHL pars accessorius described for
Colius by Berman and Raikow (1982).
DISCUSSION
INDIVIDUAL VARIATION
Individual variation in the hindlimb mus-
culature may be summarized as follows.
M. iliofemoralis externus.--This muscle was
present in one specimen of Dicrurus, and absent
in the other.
M. flexor cruris lateralis.--In Merops albicollis,
four variants were found in five specimens: ten-
don G and pars accessoria (FCLA) absent (one
specimen); tendon G present, FCLA absent (one
specimen); tendon G and very small FCLA pres-
ent (one specimen); tendon G and small FCLA
present (two specimens). In M. viridis, three var-
iants were found in five specimens: tendon G
and FCLA absent (one specimen); tendon G
present, FCLA absent (three specimens); tendon
G and very small FCLA present (one specimen).
In M. apiaster, two variations occurred: tendon
G present, FCLA absent (two specimens); ten-
don G and small FCLA present (three speci-
mens). In Eurystomus orientalis, two variants were
found in two specimens. In both, a robust FCLA
was present, but in one, FCLA inserted only in
the intercondylar region, while in the other,
the insertion was in the intercondylar region
and on the fernoral shaft. Berman et al. (1990)
and Raikow et al. (1990) found FCL to be robust
and lacking individual variation in the species
they examined.
M. iliofemoralis.--This was present in one
specimen of Artamus leucorhynchus, but absent
in the other.
M. flexor digitorum longus.--In Artamus leuco-
rhynchus, a moderate-sized fernoral head was
present in one specimen, but absent in the oth-
er. In Dicrurus hottentottus, a large femoral head
was present in both specimens, but it was nearly
twice as large in one specimen as in the other.
M. extensor proprius digiti III.--In Merops al-
bicollis, two specimens had a double tendinous
insertion, and three had a single insertion.
Variations in muscle length or size.--The follow-
ing muscles varied in length within species (de-
tails available from author): GL, GM, PL, FPPD2,
FPPD3, FPD2, FPD3, FPD4, EDL, FHB, ABD4.
OLD varies in size in Terpsiphone mutata.
Anomalies.--In Galbula ruficauda, one speci-
men had an unknown muscle arising from the
same tendon as FPD2 and inserting onto the
tendon of insertion of FPD3 as does FL; the
latter muscle is absent in Galbula. One specimen
of Eurystomus orientalis had an extra intrinsic
foot muscle to digit II; both specimens had an
extra extensor for digit III.
BEHAVIORAL CORRELATES AND
HISTORICAL ANALYSIS
Aerial foraging and intraspecific variation in
FCL.--The qualitative intraspecific variation
found in this study (i.e. the variation in pres-
ence or absence of muscle parts within species)
is almost exclusively in FCL. This was also the
most variable muscle in the tyrant flycatchers
(McKitrick 1985, 1986). Most of the within-spe-
cies variation in the muscle in this study, how-
ever, was limited to members of the genus Me-
rops. Individual bee-eaters had: (1) no FCLA; (2)
tendon G but no FCLA fibers; or (3) tendon G
and a small FCLA.
Bee-eater species show fewer variations in FCL
than some tyrannid flycatchers (McKitrick 1986:
table 1). However, although the extremes of
variation in bee-eaters do not match those found
in tyrannids, they are greater than those found
in any other nontyrannid, and the variation in
Merops is no less remarkable than that within
species of flycatchers.
Aerial foraging and interspecific variation in FCL.--
FCL consists of two parts in many birds, a pelvic
and an accessory part. The accessory part is usu-
ally large and inserts extensively on the fernoral
shaft (George and Berger ! 966, McKitrick 199 !).
Out of nine groups showing kingbirdlike aerial
behavior, six showed a reduction in size of FCLA;
the exceptions were the jacamar Galbula, the
roller Eurystomus and the wood-swallow Arta-
mus. The jacamar had a robust FCLA, while the
roller and wood-swallow had a large FCLA that
had no insertion on the femoral shaft except in
one specimen. The control species Terpsiphone
had a robust FCLA as did the species examined
by Berman et al. (1990) and Raikow et al. (1990).
The sample size of species is small, but only
because the sample in nature also is small. Judg-
ing from the results of my study, the morphol-
ogy of FCL is moderately correlated with the
aerial foraging habit. Highly aerial birds such
as swifts lack FCLA, and in swallows the FCLA
is greatly reduced. FCL is entirely absent in
hummingbirds (Zusi and Bentz 1984). There-
fore, it appears that one can predict the mor-
phology from behavior, and reduction has oc-
curred independently in a variety of unrelated
taxa. Some species exhibiting moderately aerial
behavior (i.e. they catch prey on the wing but
do not spend most of their time in the air),
however, such as jacamars, rollers and wood-
swallows, do not have reduced morphologies
of FCL, whereas others such as bee-eaters and
drongos do.
In Dendrocolaptidae, Raikow (pers. comm.)
has found a trend toward reduction in FCLA,
with a corresponding diversion of the fibers of
FCLP to tendon M. Thus, some of the force of
FCL is exerted on the tibiotarsus rather than the
femur, which may be related to the birds' ver-
tical climbing habits and the importance of flex-
ing the hindlimb to prevent failing backwards.
I have detected no such modifications in any of
the birds with reduced FCLA examined here.
Historical analysis of interspecific variation in
FCLA.--Stronger and more meaningful state-
ments about the significance of reduction in
FCLA may be made if one compares morphol-
ogy and ecology within a phylogenetic context,
as Donoghue (1989) has done for seed plants.
McKitrick (1991) analyzed hindlimb-muscle
variation, including that of FCLA, in 103 avian
taxa, and some of the taxa examined in the pres-
ent study were included in that analysis. Tree
! from McKitrick (1991) is depicted in Figure
Fig. 2. Cladogram (from McKitrick 1991) showing occurrence of aerial foraging behavior (heavy black
lines) and hypothesized transitions in M. flexor cruris lateralis. Character 1 is FCL pars accessoria (presence
= 0, absence = 1). Character 2 is FCL pars accessoria (unreduced = 0, reduced = 1). The designation "1:10"
indicates a transition from 1 to 0 in character 1.
191
ß Ancestor
Tinamus
1:1 -. o Diomedea
108 Oceanes
'v'[1o5rlOStlcr-- .:?
Garrodia
I---' OapUon
Proco#aria
[110 puffinus
[111 Ptorodroma
Buiweria
I Hydrobatos
-- Aotoaodytos
I Eudyptos
18 t-Mdadyptos
Sphoniscus
-- pygoscolis
Chen
I r Frogeta
I / [ .,t,--
[138 r131 1302_2,1Eurylains
I I I 81 I 1I ,1[::::
I/ / ! I [ /
,31 L,TI I 11'
Sula
Anhinga
Acciter
[145[ 43L Bubo
Polih orax
491.__ Gymrgyps
Grus
Fulica
[ Rynchops
Catharacta
[ I 11:01 I t154LBrachyrarnphus
[162 Rissa
Chlnas
Pd
172 Crax
I Defrays
176 174 La s
179 Butods
[ tmus
1891 4 Crotga
[ 87 Zenana
CHARACTER 1
node 151 0 ==> 1 node 148
node 108 1 ==> 0 node 107
node 136 1 ==> 0 node 135
node 128 0 ==> 1 P/co/des
node 158 0 --=> 1 node 157
CHARACTER 2
node 127 0 ==> 1 Amazona
node 129 0 ==> 1 Tyrannus
node 164 0 ==> 1 node 163
node 170 0 ==> 1 node 169
node 182 0---> 1 node 181
Fig. 3. Transitions in M. flexor cruris lateralis (FCL)
(ACCTRAN optimization) For: character 1, FCL pars
accessoria (presence = 0, absence = 1); and character
2, FCL pars accessoria (unreduced = 0, reduced = 1).
Arrows with double lines denote unambiguous tran-
sitions that are same for al! optimization assumptions.
Arrow with a single line (character 2 only) denotes
transitions that vary with optimization assumptions.
2. The occurrence of aerial-foraging behavior
(heavy black lines) is shown on the cladogram.
These occurrences are hypothesized to be in-
dependent at each node; however, there is some
ambiguity at nodes 137 and 136. It is equally
parsimonious to suggest either one origin of
aerial foraging at node 137 and loss at 135, or
independent origins in Glaucis and Chaetura. This
ambiguity makes little difference for the pres-
ent analysis.
The hypothesized transitions obtained for this
tree in two characters are shown on the clado-
gram (Fig. 2): (1) occurrence of FCLA (presence
= 0, absence = 1); (2) reduction of FCLA (no
reduction = 0, reduction = 1). Figure 3 sum-
marizes these transitions and indicates which
transitions are primitive and which derived with
respect to the origin of aerial-foraging behav-
ior.
Merops is not included in the cladogram, but
Maurer and Raikow (1981) noted that, among
the Coraciiformes, FCLA is absent only in Tro-
gonidae and, possibly independently, in the A1-
cedinoidea, a group that includes Meropidae
and the kingfisher group Alcedinidae. King-
fishers are essentially aerial piscivores, and Bent
(1940) gave a report of Belted Kingfishers (Ce-
ryle alcyon) also catching moths and butterflies
on the wing. Although the feet are not used for
prey capture (Johnston 1989), they are used in
the excavation of nest burrows (White 1953).
Bee-eaters also nest in burrows and use their
feet to excavate them (Fry 1972). In this case,
the members of a clade showing reduced or
absent FCLA are ecologically similar; in other
words, phylogeny, ecology (aerial behavior), and
the transformation of FCLA are coincident.
Eurystomus is represented on the cladogram
by Coraciidae at node 181. It shows a slight
reduction in FCLA, but the reduction is not at
all comparable to that found in some other aeri-
ally-foraging species examined in the present
study. Coraciidae is clustered with Chordeiles
(node 181), another aerial species that also does
not show reduction in FCLA. Thus, the aerial
habit is not coincident with significant muscle
reduction.
Swifts (Chaetura) and hummingbirds (Glaucis)
do not emerge together in the cladogram, con-
trary to traditional classifications. If this sepa-
ration is valid, then aerial behavior may be in-
dependently derived in the two groups.
However, as indicated in Figure 3, loss of FCLA
is primitive for each of these groups, so these
groups cannot be considered to provide evi-
dence for the causal loss of FCLA with the evo-
lution of aerial behavior: the muscle loss pre-
ceded the evolution of aerial behavior.
Galbula is not included in the cladogram, al-
though its relatives among the woodpeckers are
included. Galbula does not exhibit reduction of
FCLA, although like Merops and kingfishers, it
catches its prey on the wing and lives in bur-
rows that it excavates with its feet (Skutch 1937).
In this case, aerial-foraging behavior apparently
is derived, but FCLA is primitive.
Unfortunately, few passefine species are rep-
resented in the cladogram. However, of the pas-
setines whose hindlimb muscles have been
studied, most show a robust FCLA (George and
Berger 1966, Raikow 1976, 1978, 1980, 1987, Bo-
recky 1977, McKitrick 1985). The aerial passer-
ines examined in the present study (Dicrurus,
Hirundo, Artamus) are probably sufficiently dis-
tantly related that the first two can be said to
represent independent data points (see Felsen-
stein 1985) in support of the causal link between
reduction of FCLA and aerial behavior. Artamus,
however, does not exhibit reduction of the mus-
cle.
The relationship between the evolution of
aerial behavior and reduction of FCLA is sum-
marized in Table 1. It shows that there are four
independent cases where the evolution of the
aerial habit and reduction of FCLA are coinci-
dent, and five cases where the two are not co-
incident. Most strikingly, the cladogram (Fig.
2) shows that reduction or loss of FCLA is prim-
itive for many birds that are widely divergent
in the manner in which they use their hind-
limbs, such as penguins, loons, grebes, ducks,
and many procellariiforms.
Several tests of significance of association of
characters are currently available. One such test,
devised by Maddison (1990), takes into account
the entire tree topology to determine whether
the dependent variable (reduction of FCLA) oc-
curs with the independent variable (aerial-for-
aging behavior) significantly more often than
would be expected by chance. Unfortunately,
the taxa included in the present study are not
all represented in McKitrick's (1991) phyloge~
ny, and Maddison's test, therefore, is not ap-
plicable. At present, however, it is clear that,
with four cases of derived association and five
without, the aerial habit does not invariably
lead to reduction of FCLA. Evidently, it is un-
important to an aerial-foraging bird whether
the muscle is robust or reduced; once a bird
evolves this habit, the muscle may be free to
vary at random as suggested by McKitrick's
(1986, 1990b) random-variation hypothesis. This
is in contrast to the suggestion made by Regal
(1977) that loss of useless structures is brought
about by selection in response to the evolu-
tionary need for developmental "noise sup-
pression."
In making comparisons of this kind, there is
always the danger that our analogies will be
imperfect; that is, incomplete knowledge about
the ecology and natural history of the organ-
isms compared, or about the functional de-
mands on the structures, prevents us from
knowing the degree to which our comparisons
are meaningful. For example, perhaps the re-
quirements for digging burrows with the feet
do not permit reduction of FCL in some species
(although in Merops they clearly do); perhaps
other unknown functional constraints are op-
erating to balance the pressures on muscle mor-
phology imposed by the aerial habit. The temp-
tation is then strong to fall back upon the
TABLE 1. Summary of data on link between evolu-
tion of aerial habit and reduction of FCRLA. In all
cases, aerial foraging behavior is assumed to be de-
rived.
FCRLA
Primi- Primi-
tively tively Reduced
Taxon robust absent (derived)
Galbula +
Merops, kingfishers
Eurystomus, Chordeiles +
Chaetura
Glaucis
Hirundo
Dicrurus
Artamus +
+
+
+
+
In three states, respectively, of FCRLA. Association of morphology
and behavior: absent; present but not derived; present and derived.
questionable concept of "phylogenetic con-
straint" to explain the messy details of the pic-
ture that emerges (McKitrick in press). In order
to maximize our understanding of such prob-
lems, a research program integrating ecology,
functional morphology, and phylogenetic sys-
tematics is needed (Wake 1991). In the mean-
time, however, it is clear that attempts to make
comparisons across species are most meaningful
when done within a phylogenetic context, so
that the details of character transformations can
be observed. Despite the hazards of generaliz-
ing across species that differ in many ways, this
approach allows one more clearly to identify
the problems in comparisons and, thereby, to
inch towards the truth. The current truth ap-
pears to be that the origin of aerial-foraging
behavior and reduction or loss of FCL are not
causally related.
ISSUE OF CIRCULARITY
The notion has been raised numerous times
that characters whose evolution one wishes to
study should not be included in any phylogeny
that forms the framework for such research (e.g.
Brooks and McClennan 1991). I cannot agree
that there is any circularity in such a method.
A phylogenetic analysis based on any character
system is a hypothesis about the evolution of
that system. It is almost incidental that the names
of the organisms that own those characters are
printed at the branch tips of the resulting clado-
grams. An alternative to using this type of anal-
ysis in the study of character evolution is to use
a tree derived from a different group of data
sets and then optimize the muscle characters
(in this case) on a tree derived from other data.
This practice will not itself lead to unambiguous
hypotheses about character transformation,
however; selecting among possible alternative
transition patterns still involves a parsimony
procedure. Presumably, all character sets are
more or less equal in their potential to yield
historical data; if they are not, only a phyloge-
netic analysis will reveal this. If one believes
that the best phylogenetic hypotheses are those
based on as much information as possible, then
eliminating data from one's analyses would be
counterproductive, especially when there are
so few cases where multiple, large data sets are
available for the same group of taxa.
INDIVIDUAL VARIATION AND
PHYLOGENETIC ANALYSIS
Most of the individual variation in the hind-
limb musculature of the specimens examined
falls into the category of "minor variants" as
described by Raikow et al. (1990). These include
variations in size and shape that are noteworthy
but are not useful for phylogenetic analysis. If
such variants were interspecific rather than in-
traspecific, they would certainly be phyloge-
netically informative; only dissection of series
can reveal this, but it is beginning to be evident
that such within-species variation can be ex-
pected in specific muscles.
The presence or absence of entire muscles is
noteworthy. Few muscles varied intraspecifi-
cally in whether or not they were present; these
were Mm. iliofemoralis (ILF), iliofemoralis ex-
ternus (IFE) and flexor cruris lateralis pars ac-
cessoria (FCLA). ILF was found in one specimen
of the wood-swallow Artarnus; it also was found
on one side of a specimen of Artamus by Raikow
et al. (1979). Further dissection would be need-
ed to determine which condition is typical for
the species.
IFE was present in one specimen of the dron-
go Dicrurus. This muscle is absent in most mem-
bers of the Passeriformes, but Raikow et al. (1979)
found IFE typically to be present in the passer-
ine bowerbird assemblage (Ptilonorhynchidae,
Callaeidae, Paradisaeidae). They also found the
muscle occasionally to be present as an anomaly
in some species of starlings (Sturnidae), a group
thought by Borecky (1977) to be the sister group
to the bowerbird assemblage. These groups are
placed relatively close together in the Peters'
Check-list (Mayr and Greenway 1962); Sibley et
al. (1988) placed them all in the Parvorder Cor-
vida, along with Dicruridae. Raikow et al. (1979)
suggested that the genetic information for de-
velopment of IFE is suppressed in most passer-
ines, and that the tendency for its reactivation
may have been present in the ancestors of the
group that includes starlings and bowerbirds.
The reactivation may then have become per-
manent in the latter group, but not the former.
The same could apply to drongos; however, in-
sufficient data are available on the distribution
of IFE in this group to state with certainty that
absence of IFE is typical of drongos.
FCL, as stated above, may vary within species
in the presence or absence of pars accessoria,
and dissection of series is necessary to deter-
mine if there is a species-typical condition. Ecol-
ogy may have an influence on the morphology
of this muscle, but the morphology is likely to
have a strong phylogenetic component as well
and, therefore, may be useful in constructing
hypotheses of relationship.
I concur with Raikow et al. (1990) in their
recommendations for the use of limb-muscle
data in phylogenetic analysis. Bilateral or mul-
tiple dissections, if possible, will greatly reduce
the likelihood of mischaracterization of the limb
musculature for any given species. Berman et
al. (1990) found "novelties" in four hindlimb
muscles in House Sparrows (Passer domesticus)
that were well represented in a large sample,
suggesting that some "errors" would still be
likely in studies relying on dissection of one or
a few specimens. Dissection of series of one or
a few reference species, therefore, is essential,
but for the most part the muscles that will vary
intraspecifically are predictable. Furthermore,
the one muscle that is most likely to vary within
species that typically exhibit aerial behavior,
namely M. flexor cruris lateralis, is situated such
that it can be easily examined in multiple spec-
imens with a mimimum of damage to the spec-
imens.
ACKNOWLEDGMENTS
I thank the following institutions and individuals
for the loan of specimens under their care: G. S. Cowles
(British Museum of Natural History); S. Lanyon, D.
Willard and S. Goodman (Field Museum of Natural
History); R. Johnston (Museum of Natural History,
University of Kansas); M. Louette (Musee Royal de
l'Afrique Centrale); D. Niles (Delaware Museum of
Natural History); D. S. Wood (Carnegie Museum of
Natural History); and R. L. Zusi (National Museum
of Natural History). P. C. Chu, S. M. Lanyon, R. J.
Raikow, G. D. Schnell and an anonymous reviewer
read the manuscript and offered many useful sug-
gestions. M. Van Bolt prepared the muscle drawings.
This study was supported by grant BSR-9006208 from
the National Science Foundation.
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APPENDIX. Specimens dissected.
Chordeiles minor, USNM 506049, 506050, 506055,
506056 (National Museum of Natural History). Merops
viridis, DMNH 61293, 61297, 61310, 61313, 61324 (Del-
aware Museum of Natural History). M. apiaster, USNM
538004, 539921, 540150, 540153 (National Museum of
Natural History). M. albicollis RG 121.66, 121.170,
121.171, 121.174, 121.179 (Musee Royal de l'Afrique
Centrale). Eurystomus orientalis, BMNH 1925.11.1.85,
1925.11.1.87 (British Museum of Natural History).
Chaetura pelagica, KU 039842, 039848, 039849, 039858,
039861, 039862, 039864, 039866 (Museum of Natural
History, University of Kansas). Galbula ruficauda,
BMNH 1932.2.3.1,1932.2.3.2 (British Museum). Dicru-
rus hottentottus, BMNH 1940.12.8.345, A/1971.3.5
(British Museum of Natural History). Artamus leuco-
rhynchus, BMNH A/1969.15.420, A/1969.15.421 (Brit-
ish Museum of Natural History). Hirundo rustica, CM
2487, 2642, 3501 (Carnegie Museum), UMMZ 225,913,
225,914, 226,243, 226,783 (University of Michigan
Museum of Zoology). Terpsiphone mutata, FMNH
345895, 345916, 345918, 345921, 345924, 345928, 345927
(Field Museum of Natural History).