AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY83:373-393 (1990)

The VCL Hypothesis Revisited: Patterns of Femoral Morphology

Among Quadrupedal and Saltatorial Prosimian Primates
ROBERT L. ANEMONE
Department of Anthropology, State University of New Yorh, Geneseo, New
York 14454

KEY WORDS Functional morphology, Vertical clinging and

leaping, Positional behavior
ABSTRACT The descriptive and functional morphology of the postcra-
nium of the vertical clinging and leaping prosimians is of great interest in both
adaptational and phylogenetic studies of extant and extinct primates. An
analysis of patterns of femoral morphology among quadrupedal and saltatory
living prosimians indicates the presence of at least two, and possibly three,
distinct femoral adaptations to the demands of an arboreal, saltatory exis-
tence. Osteological measurements were taken on 277 postcranial skeletons
representing eight prosimian families, with skeletal trunk length (Biegert and
Maurer, Folia Primatol. 17:142-156,1972) used as an estimator ofbody size in
both bivariate and multivariate (discriminant function) statistical analyses.
Whereas all extant vertical clingers and leapers share certain femoral traits
(i.e., long femur, proximally restricted trochanters, ventrally raised patellar
articular surface), Galagidae and Tarsiidae share features of the proximal
femur (i.e., cylindrical head, large posterior expansion of articular surface onto
the neck) that clearly distinguish them from the specialized leapers of the
Malagasy Republic (Indriidae and Lepilemur). These latter animals closely
resemble active quadrupedal Lemuriformes in possessing spherical femoral
heads, with little posterior expansion of articular surface and a distinctive
greater trochanter shape. Some traits suggested as being characteristic of
vertical clingers and leapers (i.e., deep femoral condyles facing posteriorly,
narrow patellar groove with prominent lateral margin, greater trochanter
overhanging anterior aspect of shaft) are shown to be common to all prosrmi-
ans except the slow-climbingiorisids. The functional significance of aspects of
femoral morphology among saltators is discussed, along with the relevance of
these results to an assessment of vertical clinging and leaping among extant
and extinct primates.

The existence among extant prosimian
rimates of extremely proficient bipedal
a
reapers has been reco ized for well over a
century (Murie and ivart, 1872). In 1967,
Napier and Walker wrote a seminal article
on prosimian locomotion in which they pre-
sented what has become known as the verti-
cal clinging and leaping (henceforth VCL)
hypothesis. The publication of this hypothe-
sis provoked a resurgence of interest in the
anatomy, ecology, and evolution of the pro-
simians, especially of those prosimians
adapted to a saltatory existence.
The VCL hypothesis can be broken down
into three components that I refer to as
behavioral, morphological, and paleontolog-
ical (Walker, 1967, 1974, 1979; Napier and
Walker, 1967). The behavioral component
posits the existence of a grou of living ro-
P
simians that share a mode o positiona be-
havior (used in the sense of Prost [19651 to
Q
include locomotor and postural behaviors),
which includes clinging in an upright pos-
Received October 31,1988; accepted February 7,1990.

@ 1990 WILEY LISS,INC

374 R.L. ANEMONE

ture to vertical arboreal supports and leap- as vertical clingers and leapers. Stern and
ing, pro elled entirely by the hindlimbs, be- Oxnards (1973)consideration of the primate
R
tween t ese supports. When on the ground
these animals engage in bipedal, kangaroo-
fossil record su gested, in spite of gaps in
2
current knowle ge of postcranial morphol-
like ho in . The mor hological component ogy among the fossils, that both atterns of
R
of the #EL typothesis olds that all modern
vertical clingers and leapers share a suite of
tarsal morphology were alrea y present
among Eocene primates. One group, com-
cp
mor hological traits (mainly, but not exclu- posed mainly of members of the family Adap-
P
sive y in the hindlimb) that allows them to
en age in this unusual mode of positional
idae, appeared to resemble the living Mala-
t
be avior. The paleontological component is
the claim that the same morpholo
gasy lemurs; the other group resembled the
modern tarsiers and galagos and included
members of the family Omomyidae.
F
among modern vertical clingers an leapersfound
was also present to some extent in ail or most
In his contribution to the VCL dehatcl,
Martin (1972a:333) coined the term “hind-
of the prosimian primates of the Eocene (i.e., limb dominated arboreal locornotion” to de-
Adapidae and Omomyidae), implying that scribe the ada tive significance of the grasp-
vertical clin ’ng and leaping is the “an- ing hindliml among most prosimian
ff
cestor” of a1 modern modes of positional
behavior found among living primates. Ta-
primates. Vertical clinging and leaping was
considered to represent an extreme develop-
bles 1 and 2 contain Napier and Walker’s ment of the hindlimb dominated pattern
classification of prosimian positional behav- ractised by only a few living prosimians.
ior and the morpholo ical traits they identi- ilartin (1972a)recognized differences in tar-
tively.
8
fied as part of the V L adaptation, respec- sal elongation among these taxa and argued
that the ancestral mor hotype for all strep-
Reaction to the VCL hypothesis was rapid
and critical (Martin, 1972a; Cartmill, 1972;
f
sirhines was a relative y unspecialized qua-
drupedal form like the mouse lemur (Micro-
Szalay, 1972; Stern and Oxnard, 1973). In cebus murinus), lacking an elon ated
their cogent critique, Stern and Oxnard calcaneus and navicular, yet still capa le of%
a
(1973) argued a ainst all three components
of the VCL hypot esis. Citing both intra- and
interspecific variation in positional behav-
some degree of leaping.
Cartmill (1972, 1974a,b, 1975) discussed
the VCL theorv in the context of his critiaue
ior, they questioned the existence of a single, of the “arborgal theory” of primate orighs
coherent group of prosimians that mi ht be and questioned two aspects of Napier and
characterized as vertical clin ers anC F leap- Walker’s (1967) hypothesis in reference to
ers. McArdle’s(1981)review of;the literature the fossil evidence for saltatory habits
on prosimian positional behavior, for exam- among Eocene prosimians. The first ques-
. indicates
ple, . that the prevalence of vertical tion was whether vertical clinging postures
clrnglng and leaping VZl’kY to ‘r? enarmGus c o d 6 he inferred frem the -resen& c i f p a p -
extent between different species of GaZago. ing adaptations in the hinfiimb and pes; the
Mor hometric analyses of both hindlimb and second concerned the argument for vertical
P
fore imb dimensions supported the evidence
for behavioral variation, and led Stern and
clinging and leaping among all or nearly all
Eocene rosimians. Whereas Napier and
Oxnard (1973)t o suggest the existence oftwo
r
ou s of saltatorial prosimians,
i
distinguis ed y the presence (Galagidae,
different
a
Walker 8967) linked graspin adaptations
in primate cheiridia with an abitual reli-
ance on vertical ostures among saltator
Tarsiidae) or absence (Indriidae, LepiZernur)
of extreme elongation of the calcaneus and
P
animals, Cartmil (1974b:67) offered an a f
ternative explanation as part of his “visual
navicular bones of the tarsus. Morphometric predation” hypothesis:
analyses of the postcranial morphology of
prosimian primates by Oxnard and cowork-
ers confirmed these results (McArdle, 1981; The combination of a grasping first toe with a
nonopposable thumb is not correlated with vertical
Oxnard et al., 1981a,b), and recent work by din ‘ng and leaping. . . it is found among didel-
Oxnard (1984) emphasizes the morphologi- [hi% and other arboreal mammals that clearly
cal uniqueness of Tarsius and thus suggests ave no indriidlike or tarsierlike ancestors. It
makes more sense to interpret the grasping foot as
the existence of a third morphological at-
tern among animals classified by Wa ker
(1967, 1974) and Napier and Walker (1967)
P an adaptation to prolonged or cautious movement
among slender branches and vines, in didelphids
and early prosimians alike.
 FEMORAL MORPHOLOGY AMONG PROSIMIANS
With res ect t o the question of vertical
B
clinging an leaping among Eocene prosimi-
ans, Cartmill (1972, 1974a, 1975) agreed
that the postcrania of the adapids Notharc-
tus and Smilodectes resemble modern Indri-
idae but ar ed that most of the Omomyidae
Y
(except per aps the necrolemurines, which
resemble Tarsius) are similar postcranially
to the primarily uadrupedal Cheirogalei-
1
dae. Like Stern an Oxnard (19731, Cartmill
(1972, 1974a, 1975) distin ished between
li”
two different morphologica patterns among
modern prosimian leapers, one character-
ized b elonwted tarsall elements !Ga!agidae
and $arsii$ae) and the other lacking this
specialization (Indriidae and Lepilemur),
with both patterns already separate and
identifiable in the Eocene.
Szalay’s (1972) contribution to the VCL
debate also concerned the prevalence of ver-
tical clinging and leaping among fossil pro-
simians. While noting that some Eocene pro-
simians are correctly identified as vertical
clingers and leapers (among them Smilo-
dectes, Notharctus, Herniacodon, Necrole-
mur, and Microchoerus), Szalay (1972) dem-
onstrated that saltatory locomotion was far
from ubiquitous among primates of the
Eocene, and was not present in the earliest
postcranially known primate, Plesiadapis,
an arboreal, quadrupedal, clawed climber
(Szalay and Decker 1974). Szalay (1972)
noted that an obvious prerequisite to our
understanding of the prevalence of vertical
clinging and leaping in the fossil record is the
findin of clear associations between behav-
f
ior an morphology among its living practi-
tioners. In a pessimistic but accurate s u m
mary, Szalay (1972:33) stated:
The osteological characters that might be invari-
ably associated with vertical clinging and leaping
have not been deduced as yet, if such clear-cut fea-
tures exist at all.
Recent work has improved our under-
standin of these associations in several an-
f
atomica areas. Although the metric and bi-
omechanical differences between the foot
skeletons of galagids and tarsiids and those
of indriids and lepilemurids have been well
documented (Schultz, 1963a,b; Hall-Craggs,
1965a,b; Jouffroy, 1975; Jouffroy and Les-
sertisseur, 1979; Gebo, 1985, 1987a; Gebo
and Dagosto, 1988; Anemone, 19881, the
comparative and functional anatomy of the
femur in extant prosimians has been less
well studied (Jouffroy, 1975; Jouffroy and
375
Lessertisseur, 1979; McArdle, 1981; God-
frey, 1988; Anemone, 1988). Szalay and
Da osto’s (1988:27) analysis of prosimian
geCfa1 anatomy stresses the importance of
rapid, successive, leaping and landing with
a habitual grasp (i.e., gras leaping)” among
both living prosimians anc f the common an-
cestor of the euprimates. Both Szalay and
Dagosto (1980, 1988) and Covert (1985,
1988) acknowled e the importance of leap-
ing (as well as cfimbing and quadrupedal-
ism) in the evolution of primate locomotion
but question the necessary association of
leaping with vertical clinging suggested by
Napier and Walker (1967).Gebo’s investiga-
tions of form-function relations in tarsiers
(Gebo, 1987a), indriids (Gebo and Dagosto,
1988),and other primates (Gebo, 1985,1986)
have considerably advanced our under-
standing of the diversity of pedal adapta-
tions in arboreal primates. In an innovative
application of regression anal sis, Godfrey
P
(1988) has recently examined emoral anat-
omy among Mala asy lemuriformes (also see
5
Godfrey, 1977). he suggests that, among
Malagasy prosimians, both specialized leap-
ing and quadrupedal climbing evolved sev-
eral times from a generalized ancestral form
capable of leaping, climbing, and hindlimb
suspension.
In this article, I present the results of
investigations of femoral morphology among
extant prosimians desi ed to test the mor-
f P
hological com onent o the VCL hypothesis.
am intereste(P in determining whether the
atterns of femoral morphology that emerge
P rom such an analysis support the behav-
ioral category of vertical clinging and leapin
as defined by Walker (1967, 1974) an
Napier and Walker (1967) (see Table 1).Do
8
all extant vertical clingers and leapers share
the same femoral morphology (see Table 21,
or can we distinguish between two or more
clear1 different anatomical adaptations to
i
an ar oreal, saltatory way of life? Can spe-
a
cialized leapin prosimians be consistent1
separated on t e basis of femoral morphol
from active quadrupedal taxa (sensu
F alker, 19741, most of whom also leap to
some extent? Finally, what is the functional
significance of the patterns of femoral mor-
phology found among specialized, leaping
prosimians?
MATERIALS AND METHODS
A total of 277 prosimian skeletons repre-
senting eight families and 16 genera were
376 R.L. ANEMONE

TABLE I . Classification of prosimian positional behavior'

Active quadrupedalism
Lemuridae Lemur, Varecia
Cheirogaleidae Cheirogaleus, Microcebus, Phaner
Daubentoniidae Daubentonia
Lepilemuridae Hapalemur
Slow-climbing quadrupedalism
Lorisidae Loris, Nycticebus, Arctocebus, Perodicticus
Vertical clinging and leaping
Galagidae Galago
Tarsiidae Tarsius
Indriidae Indri. Avahi, Propithecus
Lepilemuridae Lepilemur
'This classification is adapted from Walker (1974) and differs mainly in the taxonomic placement of Hapalemur and Lepilurnur. Whereas
Walker (1974)classifiedtbesegenerain thefamilv 1,emuridae.1havpfnllowerl TattPrsn1l!lWV!ir glsrin_n!hcsct3~3illL~l;ibn;;;:i~;~.rP~i
a recent classification of prosimian positional hebaviora, see Gebo (198%).

TABLE 2. Morphological correlates of vertical TABLE 3. List of specimens used in this study
clinging and leaping in prosimians' i" = 2771
General and limb proportions Taxa Number
Small to medium body size
Long tail (except Indri) T u p a iid a e
High intermembral index Tupaia sp. 20
High brachial index Tarsiidae
Pelvis Tarsius sp. 8
Long ilium and short ischium Lemuridae
Prominent anterior superior and inferior iliac spines Lemur catta 5
Broad iliac blades in larger animals L. sp. 3
Narrow iliac blades in smaller animals L. coronatus 1
Femur L. rubriventer 2
Long and straight shaft L. fulvus 18
Cylindrical or spherical femoral head Varecia uariegata 12
Greater trochanter overhangs anterior aspect of shaft 41
Posterior expansion of articular surface onto neck Cheirogaleidae
Anteroposteriorly deep, posteriorly projecting condyles Cheirogaleus major 6
Narrow and deep patellar groove Microcebus murinus 20
Patellar surface projects anterior to shaft 26
Prominent lateral patellar ridge Tepilemuridae
Tibia Hnpalemur grzseus 16
Latera!iy campressed shat%
Posteriorly projecting condyles
H. simus 1
Pes Lepilemur mustelinus 21
Large and strong grasping hallux 38
Prominent peroneal tubercle Indriidae
Reduction of digits I1 and 111 Avahi laniger 9
Elongate calcaneus and navicular (in small bodied Indri indri 4
forms) Propithecus verreauxi 9
P. diadema 3
'From Napier and Walker (1967) and Walker (1974).
25
Lorisidae
Arctocebus calabarensis 4
Loris tardigradus 10
Nycticebus coucang 20
examined and measured at the American Perodicticus potto 20
Museum of Natural History in New York 54
Galagidae
(AMNH),the U.S. National Museum of Nat- Galago alleni 3
ural History in Washington, DC (USNM), G. demidoiiii 8
and the Museum of Comparative Zoology at G. crassicaudatus 24
Harvard Universitv. Cambridge. Massachu- G. senegalensis 29
setts (HMCZ) (see Fable 3). AlThou h gener- Euoticus elegantulus 1
ally considered nonprimates ampbell, 8 65
 FEMORAL MORPHOLOGY AMONG PROSIMIANS 377
1974; Luckett, 19801,tupaiids were included

imens with visible bony patholo ‘es were

never measured, some young adu ts (adult
dentition erupted but some epiphyses un-
5.l
fused) and some laboratory-reared and/or
zoo animals were used. Overall, nearly 75%
of the 277 specimens were wild-shot. The
sexes were pooled in all analyses, since pro-
simians do not exhibit significant pustcra-
nial sexual dimorphism and because many
museum specimens are of unknown gender.
The measurements taken on the femur are
described in Table 4 and illustrated in 1
Figure 1. Measurements were chosen to al-

TABLE 4. Femoral measurements

1. Femoral length; maximum length of femur from
horizontal plan of femoral condyles to most proximal
point of femur; measured between points A and B or
points H and B
2. Height of femoral head; maximum proximo-distal
length of femoral head; measured between points A
and C
3. Breadth of femoral head; maximum ventro-dorsal
length of femoral head; points of measurement not
pictured
4. Distal extent of third trochanter; maximum distance
from most proximal point of femoral head to most
distal point of third trochanter; measured between
points A and D K
5. Distal extent of lesser trochanter; maximum
distance from most proximal point of femoral head to
most distal point of lesser trochanter; measured
between points A and E 9
6. DiamPter of femoral neck; maximum proximo-distal
length of non-articular area of femoral neck;
measured between points I and J
7. Head-greater trochanter length 1; maximum
distance from most medial point of femoral head to -I I
10
most lateral point of greater trochanter in a plane
perpendicular to shaft; measured between points F
and G Fig. 1. Anatomical points of measurement on left
8. Diameter of femoral shaft; maximum ventro-dorsal femur. Ventral (1)and distal (2) views. A, Most proximal
width of femoral shaft, taken at midlength; points of point on femoral head; B, most distal point on femoral
measurement not pictured condyles; C, most distal oint on femoral head; D, most
9. Ventro dorsal length of femoral condyles; maximum distal point on third trocIanter; E, most distal point on
ventro-dorsal length of femoral condyles; measured lesser trochanter; F, most lateral point on greater tro-
between points K and L chanter; G, most medial point on femoral head; H, most
10. Mediolateral length of femoral condyles; maximum proximal point on greater trochanter; I, most distal
medio-lateral length of femoral condyles; measured nonarticular point on neck; J, most proximal nonarticu-
between points M and N lar oint on neck; K, most ventral point on femoral
1. Width of greater trochanter; maximum ventro- conlyles; L, most dorsal point on femoral condyles; M,
dorsal width of greater trochanter, taken on lateral most medial point on femoral condyles; N, most lateral
aspect of femur. Points of measurement not pictured point on femoral condyles; 0, patellar groove.
2. Head-greater trochanter length 2; maximum
distance from distal and medial point of femoral
head to most proximal point of greater trochanter;
measured between points C and H
378 R.L. ANEMONE
low the testing of hypotheses relating hind-
limb anatomy and function during ositional
behavior. They include measures o limb and
segment length, joint surface morphology,
! of isometric differences in bodily size.
and distances of muscle insertions to joint
centers. These measurements were used in
both bivariate and multivariate analyses.
One of the simplest ways of correcting for
isometric (but not allometric) aspects of vari-
ation in body size involves the use of ratios
(Oxnard, 1978; McArdle, 1981).Seven ratios
were calculated for the femoral data bee
Tables 5 and 6). The length of the femur was
frequently used as the denominator in ratios
in which the numerator is a measure of a
muscular lever arm (e.g., ratios 1, 2, 6, and
7). Since femoral length is an approximation
of the load arm of these levers, these ratios
measure the mechanical advantage of bone-
muscle systems (Smith and Savage, 1956).
The skeletal trunk length (STL) of Biegert
and Maurer (1972) has been shown to be
highly correlated with body size in both ca-
tarrhine (Biegert and Maurer, 1972) and
prosimian primates (Jun ers, 1979)and was
B
used as an estimator o body size in this
study. Relative femoral length (ratio 1)uses
TABLE 5. Distribution of femoral traits
among prosimians
Traits found among all “hindlimb dominated”
prosimians
Long and straight femoral shaft (longer in
specialized leapers)
Greater trochanter overhangs anterior aspect of
shaft
Anteroposteri.orip deep. postrri~irlyprojecting
condyies
Narrow and deep patellar groove
Prominent lateral pateller ridge
Traits found among all VCL prosimians
All traits characterizing “hindlimb dominated”
prosimians
Patellar articular surface projects anterior to shaft
Small third trochanter and trochanteric fossa and
large fovea
Traits found among Galagidae and Tarsiidae
All traits characterizing VCL prosimians
Cylindrical femoral head
Posterior expansion of articular surface onto
femoral neck
Greater trochanter tapers distally to form small
third trochanter
Traits found among Indriidae and Lepilemur
All traits characterizing VCL prosimians
Spherical femoral heading lacking subtantial
posterior expansion of articular surface (shared
by all Lemuriformes)
Medially “notched” appearance of greater
trochanter (shared by all Lemuriformes)
STL as the denominator to measure the
relative length of the femur free of the effects
In addition to the bivariate analyses de-
scribed above, multivariate statistics were
used to determine whether all vertical cling-
ers and leapers share the same patterns of
femoral morphology. Since the aim was to
compare the relative positions in multivari-
ate space of groups of prosimians defined on
the basis of positional behavior, the appro-
priate statistical techni ue was discrimi-
1
nant analysis. Multiple iscriminant func-
tion analysis IS a muitivariate technique
that allows discrimination between two or
more groups on the basis of a series of predic-
tor variables. The value of discriminant
analysis can be plain1 seen in the reduction
g
of dimensionality oft e data from the num-
ber of variables or groups to two or three
discriminant axes, which generally account
for most of the between-group variation.
Two key aspects of the interpretation of
the results of multiple discriminant analysis
are the determination of the relative impor-
tance of the predictor variables in the se a-
ration along each discriminant axis an of cp
the functional significance of those traits in
the living animal (Kowalski, 1972). Three
methods have been used to evaluate the
contribution of individual predictor vari-
ables (Anemone, 1988). Concordance be-
tween the three methods fosters eater con-
f-
fidence in the interpretation, w ile serious
discordance argues for caution in inter ret-
P fl
ing the significance of redictor varia les.
The first method is simp y to rank the impor-
tance of the predictor variables by the order
in which they are entered into the stepwise
discriminant analysis. The stepwise dis-
criminant algorithm adds variables in the
order in which they best discriminate be-
tween groups. Another possible indication of
the contribution of different variables to the
discrimination is in the relative magnitude
of their canonical coefficients. The final
method, and perhaps the most intuitive, is to
examine the correlations between each pre-
dictor variable and the various discriminant
functions or axes. The highest absolute cor-
relations are considered to indicate the most
important variables for a particular discrim-
inant axis, with a minimal r value of 0.30
bein judged significant (Tabachnick and
Y
Fide 1, 1983). In the discussion that follows,
all three methods are used in an attem t to
evaluate the relative contributions o therp
 F E M O W MORPHOLOGY AMONG PROSIMIANS 379
TABLE 6 Sample SLZPR, mrans, standard deviations, and standard errors of the mean f o r s e w n femoral
ratios b y f a m i l y
Taxa’

Sample sizes 24 :18 40

1. Relative femoral length2

Mean .426 562 .738 .711 ,519 .478 ,377 ,349
S.d. ,045 .057 ,027 ,034 ,018 .OM .023 .013
s.e.m. ,006 .007 ,010 ,007 .005 ,004 .004 .003
2. Hip flexor index3
Mean ,181 ,161 .136 .129 ,148 .167 .180 ,188
S.d. ,033 ,018 ,006 .013 .009 .012 ,012 ,014
s.e.m. ,005 ,002 ,002 .003 .002 ,003 ,004 ,003
3. Gluteal index4
Mean ,156 lL3 .IVY .I ZY .14u .Ibb .ISb .Y4Z
s.d. ,021 ,020 ,006 .017 ,012 ,012 ,008 ,028
s.e.m. .004 .003 .002 .003 ,002 .004 .002 ,002
4. Condylar index5
Mean ,840 1.08 1.17 1.12 1.10 1.01 1.03 .914
S.d. .051 ,057 ,060 .lo4 ,030 ,035 ,036 .040
s.e.m. ,007 ,007 .023 .021 ,007 ,009 ,010 .009
5. Femoral head index6
Mean .933 ,897 .921 .976 ,977 ,967 .980 .979
S.d. .025 ,049 .031 ,019 ,025 ,024 .028 ,023
s.e.m. ,003 .006 ,012 .004 ,005 ,007 .010 .005
6. Greater trochanter index l7
Mean ,155 ,150 ,141 ,154 .161 .I82 .177 .189
S.d. ,022 ,012 ,006 ,008 .008 ,008 .008 .010
s.e.m. .003 .001 ,002 ,002 .002 .002 .002 .002
7. Greater trochanter index 9
Man ,132 ,115 ,124 ,112 ,127 .139 .136 .166
S.d. .020 ,018 nnc
.-“I ,006 ,005 .007 ,008 .011
s.e.m. ,003 ,002 ,001 ,001 ,001 .002 .002 .002
‘LOR, Lorisidae; GAL, Galagidae; TAR, Tarsiidae; IND, INdiidae; LEP, lepiiemuridae, LEM, Lemuridae; CHE, Cheirogaleidae; TUP,
’f’upaiidae.
,JFemurlength/STL.
4Lesser trochanter length/femur length.
SThird troehanter length/femur length. Sample size for Lorisidae is 34, since Nycticebus (N 2 201 lacks a third trochanter.
6Condylar depth/condylar beneath.
?Head height/head breadth.
*Head-greater trochanter l/femur length.
Head-greater trochanter Z/femur length.

different variables to the overall separation
provided by the discriminant analyses.
Since animals vary in body size, and since
many aspects of shape are correlated with
size, there is a real need to be able to sepa-
rate size-dependent from size-independent
aspects of morphology in multivariate statis-
tical analysis. Many investigators have gone
to great lengths, using complicated mathe-
matical a proaches, to “correct” for differ-
1
ences in ody size (e.g., Corruccini, 1972,
1973;Manaster, 1979). I have chosen t o use a
different method in an attempt to control for
the great range in prosimian body size. The
multivariate anal ses were done on three
6”
different sets of ata: raw data, log-trans-
formed data, and finally simple ratios using
the skeletal trunk length (Biegert and Mau-
rer, 1972) as the denominator. The SPSS
package of statistical programs was used in
this study (Nie et al., 19751,and the results
of the discriminant analyses performed on
each of the three data sets are illustrated
(see Fig. 3) and are discussed below.
RESULTS
Femoral morphology
Among alagos and tarsiers (Fig. 2D,E)
the femoragl shaft is long, straight, and slen-
der. The head is cylindrical, with a flattened
medial end set on a short and thick neck
nearly perpendicular to the shaft (Walker,
1967,1974; Grand and Lorenz, 1968; McAr-
dle, 1981; Anemone, 1983, 1988). The cylin-
drical shape of the femoral head results from
the extreme degree of posterior expansion of
380 R.L. ANEMONE

Fig. 2. Ventral and dorsal views of prosimian proxi-

mal femora: Propithecus verreauxi (A), Lepilemur mus-
telinus (B), Lemur catta (C), Galago crassicaudatus (D),
Tarsius spectrum (E).
 FEMORAL MORPHOLOGY AMONG PROSIMIANS
the articular surface of the head onto the
dorsal as ect of the neck. This trait is best
B
develope among Galagidae, Tarsiidae, and
the slow-climbing Lorisidae and is in direct
contrast to the condition seen among all
Lemuriformes. The greater trochanter ex-
tends roximally to the same level as the
P
femora head among galagos and tarsiers.
Anteriorly, the greater trochanter over-
han s the ventral aspect of the femoral
B
sha t. Its widest point is proximal, and it
tapers in width distally to form a small third
trochanter. Medially, the prominent lesser
trochanter may extend as far a; the medial
edge of the head. The fovea ca itis femoris is
P
large, and the trochanteric ossa is small.
The distal femur bears tibial condyles that
are very deep and that project
The patellar oove is narrow an
a large arc o?t curvature, and is
the anterior level of the shaft. Both patellar
ridges are pronounced, but the lateral is
especially prominent (Walker, 1967, 1974;
McArdle, 1981; Anemone, 1983,1988).
Indriidae and Lepilemuridae
Amon%
(Fig. 2A, ), the femoral head is spherical and
+
is set on a short, thick neck, which meets the
shaft an an obtuse an le (Jouffroy, 1962,
1975; Godfrey, 1977). here is only a very
slight posterior expansion of articular sur-
face onto the femoral neck. As in galagids
and tarsiids, the greater trochanter over-
hangs the ventral aspect of the shaft. At its
proximal end, the greater trochanter ex-
tends medially over the neck, giving this
region a distinctive “notched appearance
that is resent in all Lemuriformes (Fig.
2A-C). $he greater trochanter is semirect-
angular, with a straight horizontal distal
edge that is clearly separated from the small
third trochanter. The lesser trochanter is
thin but elongate and never protrudes as far
medial1 as the femoral head. The fovea
P
capitis emoris is larger and the trochanteric
fossa smaller among indriids and Le ilemur
than among other Lemuriformes. 8istallr
the femoral condyles are both mediolateral
broad and dorsoventrally deep, with posteri-
or1 facing tibial articular surfaces. The pa-
9
tel a r groove is narrow and deep, with prom-
inent medial and, especial1 , lateral ridges.
The patellar surface extendys through a sub-
stantial arc of curvature and is raised ven-
tral to the level of the femoral shaft.
Although all vertical clingin and leaping
f
prosimians do share a series of emoral traits
that may be related to aspects of locomotor
381
a
behavior (e. ., long femur, greater tro-
chanter over anging ventral femoral shaft,
narrow patellar groove with rominent lat-
P
era1 ridge, deep femoral condy es with oste-
riorly facing tibial articular surface$, the
eat majority of these traits can also be
gund among active quadrupedal lemuri-
formes. Consequently, these traits are poor
redictors of positional behavior and may be
getter considered as characteristic of “hind-
limb dominated prosimians (Martin,
1972a). The only femoral trait that consis-
tently links all vertical clingers and lea ers
and unequivocally distinguishes theni 11 ? ulii
4
active quadrupeds (locomotor groups as de-
fined in Table 1)is the possession amon the
specialized leapers of a ventrally raise gf pa-
tellar articular surface. Additional traits
that tend to distinguish, albeit with much
less precision, between leapers and quadru-
peds include a small third trochanter (al-
thou h this is also characteristic of lorisids),
7
m a 1 trochanteric fossa, and a large fovea
capitis femoris. Alternatively, several traits
of the proximal femur lend strong su
the case for the presence of two i ferentgportto
morphological patterns among leaping pro-
simians. With res ect to the shape of the
B
femoral head, the egree of posterior expan-
sion of articular surface onto the neck, and
r
the shape of the eater and lesser trochant-
ers, galagos, an tarsiers on the one hand,
and indriids and Lepilernur on the other,
present two very different mor hological
Yi
atterns. In all of these traits, in riids and
eepilemur more closely resemble active qua-
drupedal lemurs (sensu lato) than they re-
semble galagos and tarsiers. The distribu-
tion of femoral traits among prosimian
primates classified by positional behavior is
summarized in Table 5.
Ratios
Results of the bivariate analyses of femo-
ral measurements are listed in Table 6 (by
family) and Table 7 (by genus and species).
Several of the seven ratios calculated from
the femoral measurements concern the le-
verage of various muscles actin on the fe-
gf
mur during locomotion (i.e.,hi f exor index,
gluteal index, and greater troc anter indices
1 and 2). Relative femoral length is a mea-
sure of the length of the femur relative to
skeletal trunk length. The four families that
leap most effectively and most frequently
(i.e., Tarsiidae, Indriidae, Galagidae, and
Lepilemuridae) possess femora that are
 TABLE 7. Samule sizes. means. standard deviations. and standard errors o f the mean for seven femoral ratios 3v Penus and sDecies
C,. M. Lemur V. varie- Hapa- I-. mus- A. Propith- A. cala- L. tardi- N. G. wassi- G. demi- G. sene- E. ele-
major murinus sp. gata lemur s1). telinus laniger I. indri ecus sp. barensis gradus coucang' P. potto cautlatus dovii G. alleni galensis gantulus
(N=7) (N=20) (N=29) ( N = l l ) (N=17)- tW=21) (N=9) (N=4) (N=ll) (N=3) (N=ll) (N=20) (N=20) (N.22) (N=9) (N=3) (N=28) (N=l)

1. IWative femoral
length
Mean 349 ,387 ,499 ,436 ,515 I522 ,718 .743 .693 ,415 ,506 ,409 ,400 ,517 ,492 596 ,618 ,539
s.d. ,025 ,011 ,028 ,011 .023 016 ,034 ,022 ,028 ,024 ,031 ,017 ,012 ,019 ,025 .017 ,015
s.e.m. .010 ,003 .005 ,003 .006 004 .OH ,011 .008 ,014 ,009 ,004 ,003 ,004 ,008 ,010 .003
2. Hip flexor index
Mean ,203 ,171 .I58 ,189 ,149 146 ,125 ,123 ,135 ,156 ,124 ,189 ,207 .I 82 .I61 ,165 ,145 ,159
s.d. .015 ,010 ,013 ,010 ,009 007 .016 ,010 ,009 ,014 ,012 ,009 ,011 .cog ,010 ,010 ,008
6.e.m. ,006 ,002 ,002 ,003 ,002 001 ,005 ,005 ,003 ,008 ,004 .002 ,003 .co2 ,003 ,006 .001
3. Gluteal index
Mean ,156 ,129 .I63 ,173 .154 127 ,115 .I32 ,139 .124 ,125 - ,163 ,145 ,121 ,131 ,108 ,155
6.d. ,005 ,010 ,012 .013 ,015 010 ,016 ,013 ,010 ,019 ,014 - ,009 .C 13 .010 ,016 .008
6.e.m. .002 ,002 .002 ,004 ,004 002 ,005 ,007 ,003 .Oil .005 - .002 .C$O3 ,003 ,009 ,002
4. Condylar index
Mean 1.041 1.024 1.016 385 1.044 I146 1.208 1.016 1.077 ,915 ,866 ,850 ,806 1.('23 1.044 1.107 1.130 1.123
S.d. ,032 .042 ,041 ,032 ,037 026 ,034 ,032 ,101 ,032 ,041 .044 ,041 L.20 ,034 .014 .032
s.e.m. ,012 ,009 ,008 .010 ,009 006 ,011 ,016 ,031 .018 ,012 ,010 .009 ,004 ,011 ,008 ,006
5. Femoral head
index
Mean ,951 ,994 .972 ,959 ,974 978 ,975 ,967 .980 ,933 ,952 ,916 ,939 .L128 ,922 ,910 ,863 .906
s.d. .029 .028 .019 ,030 .020 028 .019 ,032 ,013 .010 ,015 ,022 .026 ,431 ,042 ,051 ,045
s.e.m. ,011 ,006 ,004 .009 ,005 006 ,006 ,016 ,004 ,006 ,005 ,005 .006 .(I07 ,014 .029 ,008
6. Greater trochanter
index 1
Mean ,190 .171 . I 78 ,189 ,168 157 ,152 ,151 ,156 .I36 ,120 ,159 ,173 .)61 .I54 ,154 -140 ,145
s.d. ,008 ,007 .008 ,006 ,006 008 ,009 ,009 -007 ,010 ,010 .007 ,010 ,006 .008 ,016 ,006
s.e.m. .003 ,002 .002 .002 ,001 002 ,003 ,004 .002 ,006 ,003 ,001 ,002 .(I01 ,003 ,009 ,001
7. Greater trochanter
index 2
Mean ,143 ,132 ,137 ,143 ,131 123 ,108 ,113 ,114 .126 .098 ,138 .145 .I 16 ,120 ,113 .112 ,120
s.d. ,010 ,006 ,006 ,007 ,006 006 .006 ,007 ,005 .005 ,008 ,010 ,010 .( 19 ,009 .003 ,021
s.e.m. ,004 ,001 ,001 ,002 ,001 ,001 ,002 ,003 ,001 ,003 ,003 ,002 ,002 .(so4 ,003 ,001 ,004

'The gluteal index of". coucang is biank due to the lack of a third trochanter in this form.
 FEMORAL MORPHOLOGY AMONG PROSIMIANS
more than half as long as their skeletal trunk
lengths (Jungers, 1979, 1985; McArdle,
1981; Anemone, 1988). Galagidae and Lepi-
lemuridae, however, have significantly
shorter femora than do Tarsiidae and Indri-
idae. In fact, in the latter two families, femo-
ral length is more than 70% of skeletal trunk
length. There is a spectrum of decreasing
relative femoral length among the Mala asy
prosimians, ranging from Indriidae and ep-
ilemuridae to Lemuridae and Cheirogalei-
!i
dae. A similar s ectrum exists with the ge-
nus Galago, in wphich predominantly leaping
species such as G. senegalensis and G. aileni
have significantly longer femora than the
more quadrupedal s ecies (i.e., G. crassicau-
B
datus and G. demi ouii). The shortest fem-
ora among the taxa included in this study
belong to Tupaiidae, relatively unspecialized
terrestrial and arboreal quadrupeds. These
results clearly indicate that a long femur is
common among saltatorial primates. How-
ever, they also show that the degree of femo-
ral elongation varies considerabl among
B
specialized leaping prosimians an that In-
driidae and Tarsiidae are far more similar to
each other in this respect than either is to
Galagidae or Lepilemuridae.
Hip flexor index is a measure of the distal
extent of the lesser trochanter relative to
overall femoral length. Indriidae and Tarsi-
idae show the most proximally placed lesser
trochanters, followed by Lepilemuridae,
Gala 'dae (particularly G. senegalensis),
f
and emuridae (particularly Lemur sp.).
The most distally ositioned lesser trochant-
ers are to be foun(Pin the quadrupedal fami-
lies Tupaiidae, Cheirogaleidae (especiallyC.
major), and Lorisidae. Gluteal index mea-
sures the distal extent of the third tro-
chanter relative to total femoral length. The
taxa with the most proximally positioned
third trochanters are Tarsiidae, Galagidae
(especially G. senegalensis, G. alleni, and G.
demidovii), and Indriidae, followed by
Cheiro aleidae (particularly M. murinus).
8
Tupaii ae are clearly differentiated from all
rosimians on the basis of the extremely
57istal osition of their third trochanters
8
(McAr e, 1981; Anemone, 1983,1988).
The condylar index is a ratio of the anteri-
or-posterior dimension of the femoral
condyles to their mediolateral dimension.
The only separation effected by the condylar
index is between the Lorisidae and Tu ai-
idae and all other prosimians, althoug it R
should be noted that the highest values (i.e.,
383
the relatively anteroposteriorly deepest fem-
oral condyles) are found in the four predom-
inantly lea ing families. There is no clear
\
separation etween Malagasy taxa and the
non-Malagasy leapers. Only the slow-
climbing lorisids and the unspecialized qua-
drupedal tree shrews have femoral cond les
that are wider (mediolaterally) than eep B
(dorsoventrall 1. All the Malagasy lemuri-
P
formes as we1 as the Galagidae and Tarsi-
ossess femoral condyles that are
sli ht y deeper than wide.
di: se of the femoral head indPx is an at-
tem t to quantify variability in the shape of
f
the emoral head. The results indicate a very
slight difference between, on the one hand
tarsiids and galagids and, on the other all of
the Malagas taxa and Tupaiidae. In all
K
prosimians, owever, the femoral head is
slightly larger in its dorsoventral dimension
than in its craniocaudal dimension. Signifi-
cant differences in the shape of the femoral
head, which can be clearly seen in Figure 2
(e.g., cylindrical vs. spherical shape, extent
of posterior ex ansion of articular surface),
do not reveal t!l emselves in this ratio.
The two greater trochanter indices are
measures of the distance from the hip joint to
the lateral edge of the greater trochanter
relative to femoral length. In both ratios, the
taxa with the smallest values are Tarsiidae,
Galagidae, and Indriidae. Conversely, those
taxa with relatively large values, and hence
longer moment arms, are the quadrupedal
a
Tupaiidae, Cheiro aleidae, and Lemuridae.
One exception is t e surprisingly low value
of the slow climbin Lorisidae on greater
trochanter index 1.9%is result is most likely
due to the presence of relatively long femora
among certain Lorisidae, particularly the
genus Loris. There exists a clear spectrum
a
among the Mala asy taxa from the leapin
Indriidae with t e lowest values, throug
the progressively less saltatorial Lepilemu-
a
ridae, Lemuridae, and Cheirogaleidae.
Discriminant analysis
Results are presented for the first three
discriminant axes because, in all analyses,
they account for approximately 90% of the
total between-group variance (Anemone,
1988).Bivariate plots of the mean values for
each prosimian famil on the first three
F
discriminant axes are igured for each of the
three femoral data sets (i.e., raw, ratio, and
log-transformed) used in this analysis
(Fig. 3).
384 R.L. ANEMONE

5- A 2j
* 1 -
4 - '
l'A

3 -'
0 -'
m x
Y
hl
2 -'
A M -1 -
2
x
Lo
;z -2 -
0
1 -
a
O- 6 m A
0 = -3 -'

-1 - '
-4 -

-2 -'
X -5 -
KI 6.
-6
I

-3 7
- 6 - 4 - 2 0 2 4 6 8

AXIS 1
8
5-
0 3
4 -* *
2 -'
3 -. 0 X

N 2 -. M 1 - '

-x
v)
1 -. A
A X
-x
v)
0-
0
U U
0 --
-1 -'

-1 -. B

-2 --

- 3 i i :
m
:m :
6

a;
: a ; * ,
d
-2 1
-3C--+---t--t~i
-10 -8 -6 -4 -2 0
i i

2
i
4
i
6 8

AXIS 1 AXIS 1
C
4

3 -.
* 0

2 -'
A
A
1 - '
M
N
-x
v) 0 -. 2
K
a -1 - ' Q
X
-2 -
-3 -'
U
6
-44 i 1 i i i i i i
-12-10 -8 -6 -4 -2 0 2 4 6 -12 -10 -8 -6 -4 -2 0 2 4 6

AXiS 1 AXIS 1
Fig. 3. Bivariate plots of the first three discriminant A , Lepilemuridae; , Lemuridae; x Tarsiidae; *, Tu-
axes from raw (A), ratio (B), and log ( C ) data. , + paiidae. Skeletal trunk length is the denominator in all
ratios.
Lorisidae; 0 ,Indriidae; m,Cheirogaleidae;0, Galagidae;
 FEMORAL MORPHOLOGYAMONG PROSIMIANS
The first discriminant axis indicates a
slight but consistent se aration of special-
B
ized vertical clingers an leapers (Indriidae,
Lepilemuridae, Galagidae, and Tarsiidae)
and Lemuridae from taxa with a more gener-
alized locomotor pattern (Cheirogaleidae,
Tupaiidae, Lorisidae), which, as a rule, in-
cludes quadru edalism to a greater extent
than saltation.P Tupaiidae consistently have
the lowest values on axis 1 and are most
closely approximatedby Cheirogaleidae and
Lorisidae, whereas Indriidae and, to a lesser
extent Tarsiidae, have the highest values on
axis 1. Gaiagidae are usually situated close
to Tarsiidae in an intermediate osition be-
tween the quadrupedal taxa an Indriidae.
Among the Lemuriformes a pattern is seen
rT
in which the Indriidae and Cheirogaleidae
are at opposite extremes, and Lemuridae
and Lepilemuridae span the gap between
them.
Discriminant axes 2 and 3 are not easily
interpreted on the basis of the positional
behaviors of the animals. There is neither
any apparent clustering of the lea ing taxa
on either of these axes, nor is t ere any
consistent separation of predominantly
K galagids that is much more similar to the
leaping and nonleaping forms. Malagasy
Lemuriformes are again arrayed in a spec-
trum from Indriidae, though Lepilemuridae
and Lemuridae, to Cheirogaleidae along
both axes 2 and 3. In addition, axis 3 in
both the raw and the log-transformed anal-
ysis uniquely se arates the slow-climbing
P
Lorisidae from a1 other prosimians.
Since only discriminant axis 1consistently
distinguishes between active quadrupeds
and vertical clingers and leapers, it is of
particular importance in evaluating the rel-
ative contribution of the predictor variables.
The order of entry of variables into the step-
wise analyses of the ratio and log-trans-
formed data are concordant only insofar as
femur length was the first variable entered
into each analysis. No other consistent pat-
tern a ears in the order of entry of vari-
ables. t i e relative magnitude of the canoni-
cal coefficients and their correlations also
indicate the primacy of femoral length in
determining separation along discriminant
axis 1. Other variables with high coefficients
and high correlations with axis 1 include
'Gebo (198713)suggests that the cheirogaleids possess the most
generalized locomotor patterns among the prosimians, although
he notes that Microcebus rnurinus is a competent and frequent
leaper.
385
head-greater trochanter len h 1and dorso-
8
ventral condylar length. ther variables
that may be of some importance in the dis-
crimination along axis 1 include the distal
extent of the lesser and third trochanters
and mediolateral condylar length.
DISCUSSION
Comparative analysis of the prosimian fe-
mur reveals a more complex picture than
that suggested by the VCL hypothesis (Cart-
mill, 1972; Godfrey, 1977, 1988; McArdle,
1981; Oxnard et al., 1981b;Anemone, 1983,
19861. Rather than a single morphoiogxai
adaptation to saltation among extant pro-
simians, as redicted by the VCL hypothesis,
P
the femora evidence strongly supports the
existence of two different solutions to the
problems posed by an arboreal, saltatory
existence. Although galagos and tarsiers
are, except for size and robusticity, closely
similar in femoral morphology, the lemuri-
form vertical clingers and leapers (indriids
and Lepilemur) present a distinct pattern of
femoral morphology from tarsiids and
pattern seen among the active quadrupeds of
the Malagasy Republic (lemurids and
cheirogaleids). Differences between Mala-
gasy and non-Malagasy leapers are evident
from observation of the femur, from a com-
parison of femoral ratios, and from the re-
sults of the discriminant function analysis.
Closer examination of the femoral traits
thought by Na ier and Walker (1967) to
P
make up a sing e VCL pattern (see Table 2)
indicates that these traits are found either
among both leapers and quadrupeds or
among some but not all vertical clingers and
leapers (see Table 5 ) . This conclusion is in
good agreement with those derived from
other analyses of the prosimian skeleton
(Cartmill, 1972; Martin, 1972a; Godfrey,
1977,1988;McArdle, 1981).
Distinctive traits of the proximal femur of
ala 0s and tarsiers include a cylindrical
aeadgwith a lar e expansion of articular
P
surface onto the orsal aspect of a thick and
short neck, which is nearly perpendicular to
the shaft. These traits appear to be related
and allow easy separation of Galagidae and
Tarsiidae from all Malagasy prosimians and
Tupaiidae. The crucial trait in this suite of
characteristics is the posterior expansion of
articular surface onto the femoral neck; it is
this trait that gives the head a cylindrical
shape and makes the neck appear short and
386
thick. The proximal femoral anatomy of all
Malagasy taxa, both specialized leapers and
uadrupeds, includes a spherical
active
femoral R
ead with little or no posterior ex-
pansion of articular surface. Interestingly,
galagos and tarsiers are most close1 ap rox-
imated in the shape of the femoral ea and
the configuration of its articular surface by
E l
the slow-climbinglorisids.
I interpret the articular expansion seen in
galagos and tarsiers as a postural adapta-
tion of importance during vertical clin 'ng
behavior ir, small-bodied prosimians. &ile
vertically clinging to an arboreal support,
the femora are strongly flexed, abducted,
and laterally rotated. In this position, the
posterior expansion of the articular surface
comes into contact with the distal articular
region of the acetabulum, allowing the nec-
essary posture preparatory to lea ing. Jen-
kins and Camazine (1977) similar y related
the degree of expansion of the articular sur-
P Oxnard, 1973; Petter and Peyrieras, 1975;
face of the femoral head onto the neck among
carnivores to the relative im ortance of the
use of the femur in abductec r postures. The
absence or poor development of this trait
among Indriidae and Lepilemuridae may be
the result of different hindlimb postures dur-
ing climbing or clinging among these larger
animals2 (Godfrey 19771, whereas its pres-
ence among Lorisidae may reflect the enor-
mous degree of femoral mobility in these
slow-climbing,arboreal forms.
Few traits are shared by all vertical cling-
fossa,
and a reduced third trochanter. Haii-Craggs
(1965a,b) clearly demonstrated the biome-
chanical
1982, 1988). Close examination of Tables 6
and 7, however, indicates a great deal of
interfamilial variation in relative femoral
length (ratio 1)among VCL taxa. Especially
noticeable are the differences between
Galagidae (562) and Tarsiidae (.738) and
between Indriidae (.711) and Lepilemuridae
(519). Even the most specialized leapers
among the Galagidae (i.e., G. senegalensis,
2Although most indriids are larger than most galagids and
tarsiids. size relations are reversed in Avahi Zaniger and Galago
crussicaudatus. Nowak and Paradiso (1983)state that the former
taxon ranges in body weight from 600 to 1000 g, and the latter
ranges from 1,000 to 2,000 g. Head and body length in both taxa
approximates 300 mm (Nowak and Paradiso, 1983).
R.L. ANEMONE
,618, and G. alleni, .596) have si ificantly
%?
shorter femora than tarsiids an indriids,
whereas, for less s ecialized gala 'd leapers
1
(i.e., G. crassicau atus, .517, ani l G. demi-
douii, .492),the differences are even greater
(see Table 7). Although long femora are
portance or frequency of leaping (vs. quadru-
pedal running and climbing) and historical
or heritage features. It should be noted that,
ammg the active ya.drupeda.1 [sensu
Walker, 1974) taxa, on y Hapalemur has a
femur that is half the length of its skeletal
trunk length. Not surprisingly, the locomo-
tor behavior of H. griseus apparently in-
cludes a large proportion of leaping as well as
vertical clinging postures (Na ier and
Walker, 1967;Walker, 1967,1974;i t e r n and
Gebo, 1987b).Jenkins and Camazine (1977)
found that the position of the fovea capitis
femoris, the attachment on the femoral head
for the ligamentum teres, is an indicator of
femoral posture among carnivores. This re-
sults from the restriction of the round liga-
ment to the nonarticular acetabular fossa
when the femur is abducted (Jenkins and
Camazine, 1977). Although no consistent
pattern of foveal position among prosimians
was noted in this study, the animals classi-
fied as vertical clingers and leapers appear
to have lar er foveae than animals consid-
K
ered by Wa ker (1974) to be active quadru-
peds. This relationship may have something
to do with the more frequent,use of the femur
in abducted postures among the former ani-
mals, but further research would be required
to test this preliminary hy othesis. The tro-
chanteric fossa offers attacYlment to the ten-
don of M. obturator externus, one of the
lateral rotators of the femur. The smaller
trochanteric fossae among leapers may re-
flect a reduction in the size of this muscle,
but the significance, if any, of this trait for
lea ers is unclear. The presence of a large
anIp powerful third trochanter is more com-
mon among cursorial quadrupedal mam-
mals such as horses than among saltators
and is linked to the powerful development of
Mm. gluteus superficialis and tensor fasciae
femoris as adductors of the femur (Gregor ,
1912; Smith and Savage, 1956).In his stu y
of leaping ada tations among rodents, How-
B
P
ell (1932)simi arly noted the proximal posi-
tion and reduced size of the third trochanter.
 FEMORAL MORPHOLOGY AMONG PROSIMIANS
Among both prosimian vertical clingers
and leapers and active quadrupeds, the
greater trochanter overhangs the anterior
aspect of the femoral shaft. The significance
of this trait appears to be related to the
direction of pull and associated leverage of
M. vastus lateralis, which arises from the
ventral aspect of the greater trochanter
(Walker, 1967). Comparative investigations
of the thigh musculature among both qua-
drupedal (Jouffroy, 1962; George, 1977;
Jungers et al., 1980) and saltatorial (Wool-
lard, 1925; Jouffroy, 1962; Stevens et al.,
1972, h e m a n e , 19881 prosimians indicate
that M. vastus lateralis is consistently the
largest member of the quadriceps femoris
group. Its origin is roximally restricted to
P
the ventral aspect o the reater trochanter.
Gregory (1912) showed t i a t increasin the
angle of insertion of a muscle into a longgb one
has the general result of increasing the com-
ponent of force directed perpendicular to the
shaft while reducing the joint reaction force
directed arallel to the shaft. This is the
f!
probable unctional effect of the characteris-
tic ventral overhan of the greater tro-
B
chanter. Jungers et a . (1980)demonstrated
the im ortant role M. vastus lateralis plays
in the feaping behavior of lemurids throu h
the use of telemetered electromyography. ts
large muscle mass and resultant increased
f larger relatives N cticebus and Perodicticus.
cross-sectional area and long, parallel mus-
cle fibers are clearly ada tations allowing
P
both powerful and rapid emoral extension
(Gowitzkeand Milner, 1980).However, since
these aspects of muscular morphology and
the associated shape of the greater tro-
(Szalay and Decker, 1974; Szalay and
Dagosto, 1980,1988;Covert, 1988).
Another trait of the proximal femur
shared by all vertical clingers and leapers is
the possession of proximally restricted tro-
chanters, as can be seen by examination of
the hip flexor index, gluteal index, and both
greater trochanter indices (see Tables 6 and
7). The lowest values for each of these ratios
is usually found in the specialized leaping
families (i.e., Galagidae, Tarsiidae, Indri-
idae, and Lepilemuridae), providing some
387
support for the VCL hypothesis. A closer
examination reveals, however, a more com-
lex picture with a significant degree of over-
fap between taxa identified as active quad-
rupeds and VCLs. Thus, Cheirogaleidae,
mainly on account of the low value found in
Microcebus murinus, fall within the range
of specialized lea ers with respect to the
luteal index. $he difference between
Eheirogaleus andMicrocebusclearly reflects
the greater saltator component of the loco-
E
motor behavior o f t e latter genus (Martin,
1972b; Gebo, 198713). Interspecific variation
in each of these ratios withir, the genas
Galago mirrors the spectrum of leaping abil-
ities (Charles-Dominique, 1977; Charles-
Dominique and Bearder, 1979; Crompton,
1980,1984) and other aspects of morpholog-
ical variation (McArdle, 1981; Anemone,
1982, 1988) among these species. To a
greater extent than might be predicted on
the basis of their nonsaltatory mode of loco-
motion, lorisid genera resemble leapers in
having proximally restricted trochanters,
particularly the greater trochanter. Inspec-
tion of Table 7 reveals that only the small-
bodied lorisids (i.e., Arctocebus and Loris)
have proximally restricted trochanters, as
well as relatively longer femora than their
McArdle (1981) lrst noted this dichotomy
within the lorisids, and related it to differ-
ences in habitat utilization, diet, and posi-
tional behavior. In any event, the functional
basis of proximally restricted trochanters
among some lorisids is not explicated by the
followingdiscussion of this trait among other
prosimians Ke., active quadrupeds and ver-
tical clingers and leapers).
The lesser, third, and greater trochanters
are important muscle attachment sites for
M. iliopsoas, Mm. gluteus superficialis ars
!;r
anterior and tensor fasciae femoris, and m.
luteus medius and minimus, res ectively.
P
t h e four ratios (hip flexor, glutea , greater
trochanter 1 and 2) measure the distance
from the center of the hip joint to the distal
point of each of these trochanters relative to
femoral length, Although this distance is not
a true measure of the muscular moment arm
involved,the two are closely correlated, since
the moment arm will increase as the inser-
tion is prolonged distal1 (Gregory, 1912;
K 8
Smith and Sava e, 1956; tern, 1971,1974).
Thus a proximal y restricted attachment site
(and, hence, a low value on the appropriate
ratio) results in a shorter moment arm and a
388 R.L. ANEMONE
consequent decrease in mechanical advan-
tage. As developed by Smith and Savage
(1956),the conce t of mechanical advantage
F
explains much o the variation in mamma-
lian skeletons in dichotomous fashion, as
reflecting adaptations for either power or
speed. Muscle-bone systems adapted for
power are characterized by high mechanical
advantage; those adapted for speed are said
to have low mechanical advantage. The me-
chanical advantage of a bone-muscle system
is defined as the ratio of the moment arm of
the muscular force to the moment arm of the
load or, put differently, the ratio of the lever
arm to the load arm (Smith and Savage,
1956). The dichotomy of power vs. speed in
muscular adaptation has played an impor-
tant role in this and many other studies of
mammalian functional anatomy (Hall-
Craggs, 1965a,b;Stern, 1971,1974;Jungers,
1976; McArdle, 1981). The proximally re-
stricted trochanters of vertical clingers and
leapers are clearly adaptations for s eed at
the expense of power in extension (M!m. glu-
teus medius and minimus), flexion (M. ilio-
psoas), and abduction combined with exten-
sion (Mm. gluteus su erficialis pars anterior
!?
and tensor fasciae emoris) of the femur.
Howell (1932) found that the femoral tro-
chanters of saltatorial rodents are similarly
restricted proximally.
An additional adaptive rationale for prox-
imal placement of muscle insertions on long
bones is the resultant reduction in the mass
moment of inertia of the limb (Jungers, 1976;
Gowitzke and Milner, 1980). The mass mo-
ment of inertia is, for rotational motion, the
aaaieg efmass ir:h e a r m~ticn.As s ~ c hit?is
a measure of the resistance of a body at rest
to change in angular motion and is propor-
tional both to the mass of the body and to the
distribution of mass about the axis of angu-
lar movement. Thus the mass moment of
inertia of a limb increases with increasing
distribution of its mass at a distance from the
center of rotation. With the muscular mass
proximally restricted and the mass moment
of inertia minimized, the limb can be rotated
at a greater rate by a given muscular force.
This is the same principle that allows an ice
skater to rotate uickly or slowly de ending
B P
on the distance t e arms are held rom the
body; closely for speed, further from the body
to slow down, and it is clearly of value to
saltatorial animals whose hindlimbs need t o
attain relatively high velocities during take-
off (Hall-Craggs, 1965a,b).
In his study of the hip and thigh of Lorisi-
formes, McArdle (1981) calculated similar
ratios to some of those used here. Althou h
offered the caveat that the use of femoral
Fl
my results are essentially identical to his, e
length as the denominator in these ratios
may have skewed the results, since taxa with
a parently more proximally positioned tro-
R
c anters usually have the longest femora.
There is, however, every reason t o believe
that, were it advantageous to the animals, a
lineage could increase the length of the fe-
mur while maintaining high mechanical ad-
vantage in the muscles crossing the hi joint
(i.e., distally positioned trochanters). $here-
fore, the fact that some prosimian taxa have
reduced the muscular moment arms in con-
junction with an increased functional len h
of the hindlimb is certainly significant. &e
fact that femoral elongation appears to have
taken place distal to the level of the trochant-
ers is of functional significance and should
not be ignored.
In the distal femur of both vertical clingers
and leapers and active quadrupeds, a suite of
traits appears to be linked to powerful and
efficient extension of the leg at the knee by
M. quadrice s femoris. These traits include
B
femoral con yles that are deeper dorsoven-
trally than mediolaterally wide, a narrow
and deep patellar oove bordered by a prom-
B
inent lateral pate lar ridge, and posteriorly
facing tibia1 articular surfaces. The only
trait that allows complete discrimination be-
tween specialized leapers and quadrupeds is
the raised patellar articular surface, which
is shared by all vertical clingers and leapers,
4s Walker f?9E?i first mted, deep fernera!
condyles and a raised patellar articular sur-
face are two means of increasing the size of
the “pulley” over which the quadrice s ten-
don acts and, hence, of increasing t{e mo-
ment arm of M. quadrice s femoris. This is
best interpreted as an a dpaptation for maxi-
mizing the power of leg extension at the
knee, perhaps at the ex ense of speed. Other
traits of distal femora’p anatomy are simi-
larly related to extension of the leg by M.
quadriceps femoris. The prominent lateral
patellar ridge counteracts the pull of the M.
vastus lateralis, the largest member of the
M. quadriceps femoris group in most prosim-
ians (Jouffro ,1962,19751, and thus guards
f
against pate lar dislocation during contrac-
tion of that muscle (Jungers et al., 1980).The
narrow and deep patellar groove with a large
arc of curvature is a further indication of the
 FEMORAL MORPHOLOGY AMONG PROSIMIANS
emphasis on flexion and extension at the
knee (Tardieu, 1980).These traits, as well as
the posteriorly facing tibia1 articular sur-
faces, are found among both quadrupedal
(exce t Tupaiidae) and saltatorial prosimi-
ans. hthough they are in sharp contrast to
the condition seen in the specialized slow-
climbing Lorisidae, these characteristics do
not successfully distinguish between active
uadrupedal and leaping prosimians.
lather, they form a functional complex that
includes muscular s ecializations in M.
1
uadriceps femoris ( ungers et al., 1980;
9 oaffroy 1962) and i s prnhahly associated
a
with the eneral propensity for leaping be-
haviors t at is common to both VCL and
active quadrupedal prosimians (Jouffroy,
1975).
With respect to the analytical tools used in
this study, it is clear that the results of
multiple discriminant functional analysis
were disappointing in several ways. Only
axis 1appeared easily interpretable in light
of known differences in positional behavior
of the various prosimian taxa. In addition,
the difficultiesof making causal connections
between the discrimination along any axis
and the variables responsible for that dis-
crimination are discouraging. Perha s we
have an example of “Rao’s aradox”(Epowal-
R
ski, 1972:121), in which t e simultaneous
treatment of variables that, compared
univariately, are significantly different be-
tween groups and “noise”variables that do
not differ significantlyresults in a multivari-
ate analysis with less discriminating power
than a univariate analyses of the significant
variables.
SUMMARY
It should be evident from the discussion
that all extant vertical clingers and leapers
do not share the same femoral morphology
(Cartmill, 1972; Godfrey, 1977,1988; McAr-
dle, 1981; Anemone, 1983, 1988). Although
the distal femur of all vertical clingers and
leapers is essentially similar and is likely to
represent a euprimate adaptation, there are
clear differences in the proximal femur that
allow us to distinguish the Galagidae and
Tarsiidae from the Indriidae and Lepilemur.
Two features, the shape of the femoral head
and neck and the position and shape of the
greater trochanter allow easy discrimination
between these two groups (see Fi .a). Mor-
f 7
pholo ‘cal similarities between ga agids and
tarsii s may reflect either the independent
389
acquisition of convergent leaping adapta-
tions (Szalay, 1972; Cartmill, 1972; Martin,
1972; Stern and Oxnard, 1973; Godfrey,
1977,1988; Szalay and Dagosto, 1980,1988;
Oxnard, 1984;Covert, 1988)or the retention
in these two lineages of primitive, eu rimate
adaptations (Napier and kalker,
kk$balker, 1967, 1974). The results pre-
sented here support independent acquisition
of leaping adaptations in the ancestors of
alagids and tarsiids. Sup orting evidence
cp
for this view can be adduce from a consider-
ation of the anatomical evidence of the es
and the crus among the extant forms. ?par-
sius lacks the calcaneocuboid pivot found
amon all other prosimians (Hafferl, 1929;
8
Hall- raggs, 1966; Decker and Szalay,
19741, has a unique method of foot rotation
and pedal grasping (Gebo, 1987a), and is
unique among extant primates in possessing
a fused tibia and fibula (Clark, 1971).These
differences between tarsiers and galagos
support independent acquisition of leaping
adaptations in these phylogeneticallywidely
separated taxa.
Patterns of morphology in the prosimian
femur indicate the presence of two or, more
likely, three different solutions to the de-
mands of an arboreal, saltatory existence
among prosimian primates. The galagid and
the tarsiid patterns share a c lindrical fem-
9
oral head, with a substantia expansion of
articular surface onto the distal aspect of the
femoral neck, as well as elongation of the
calcaneus and navicular (Schultz, 1963a,b;
Hall-Craggs, 1965b; McArdle, 1981; Anem-
one, 1982, 1988). Tarsiers differ from gala-
gos, however, in the possession of signifi-
cantly longer femora and more proximalig
restricted femoral trochanters as well as in
several musculo-skeletal specializations in
the foot and leg (see above). Inters ecific
cp
variation within the genus Galago in icates
the existence of a spectrum of behavioral and
morphological specializations ranging from
very s ecialized vertical clingers and leapers
B
(i.e., . senegalensis and G. alleni) to pre-
dominant1 quadrupedal taxa (i.e., G. demi-
6,
douii and crassicaudatus)(Charles-Domi-
nique, 1977; Charles-Dominique and
Bearder, 1979;Crompton, 1980,1984;McAr-
dle, 1981;Anemone, 1988)and is reflected in
the femoral ratios presented here (see
Table 7). Indriids and Lepilemurids present
a third morphological adaptation to leapin
that is characterized by a spherical femora 7
head, very long femur, absence of tarsal
390 R.L. ANEMONE
elongation (Jouffroy, 1975; Godfrey, 1977,
1988; Jouffroy and Lessertisseur, 1979;
Jungers, 1979; McArdle, 1981; Anemone,
1988), and, in common with lemurids, a s e-
cialized pedal grasping mechanism (Ge 0,
1985). In many respects (e.g., “notched ap-
t:
earance of greater trochanter, spherical
Read, narrow patellar groove), the femur
among indriids and Lepilemur resembles
that of the rest of the Malagasy lemuri-
formes: differences are quantitative rather
than ualitative (e.g., longer femur as re-
3
flecte in lower intermembral index, raised
ventral floor of patellar
The results resente$.oovej
here indicate a se-
P
ries of traits o the proximal and distal fem-
oral epi hyses among prosimians that can be
K
biomec anically related to ra id hindlimb
extension during locomotion. Long femora
with proximally restricted trochanters and
dorsoventrall deep condyles, which func-
f
tion as a pul ey, are traits that are clear1
related to leaping and that are found in a 1
“hindlimb-dominant” (Martin, 1972a) pro-
simians (i.e., all prosimians except Loris-
idae), all of which are capable of some
leaping (Gebo, 1987b). Since most of the
distinctive features appear to be related to
leaping propensities rather than vertical
clingin (except perha s the posterior exten-
rp
sion o!f articular su ace onto the femoral
neck in galagos and tarsiers), distinguishing
between Walker’s (1974) vertical clingers
and lea ers and active uadrupeds on the
P 7
basis o femoral morpho ogy presents real
problems.
In an influential paper, Bock and van
Wahlert ll965) reevaluated the cmce t ef
biological adaptation and distinguishe be-a
tween “form” and “function” of a biological
“feature.” They argued that a complete un-
derstanding of adaptive significance re-
uires an analysis of the “biologicalrole” of a
Sbrm-function complex, that is, of its use or
action in the natural environment. I have
attempted to provide just such an analysis of
the relations between form (morphology),
function (biomechanics), and biological role
(positional behavior) of the femur among
extant prosimian primates as a test of the
VCL hypothesis. It is hoped that this stud
will provide a firm basis for future wor
designed to reconstruct the biological role of
this anatomical region among extinct pri-
mates, a task made difficult by the paucity
and often fragmentary nature of fossil re-
mains.
Finally, some questions concerning the
use and validity of classifications of osi-
tional behavior can be addressed here. kot-
ing the great variability in positional behav-
ior among primates, Stern and Oxnard
(1973)suggested that the very notion of clas-
r
sif ’ng primates on the basis of ositional
be avior was doomed to failure. &houth it
is certainly true that individuals of any CL
taxon do not rely exclusivelyon saltation and
that differences in the leaping and clinging
behavior of galagids, tarsiids, and indriids
exist (Petter, 1962; Jolly, 1966; Stern and
Oxnard, 1973; Pollock, 1975, 1977; Charles-
Dominique, 1977; Richard, 1978; Niemitz,
1979, 1984; Crom ton, 1980, 19841, it does
P
not necessarily fol ow that attempts to clas-
sify prosimian primates on the basis of at-
terns of positional behavior are a hope essP
task. The classification of animals on the
basis of their dominant mode of positional
f behavior is of great heuristic value in com-
parative studies of functional morphology,
inter- and intrataxonal differences notwith-
standing. If the validity of classifications of
positional behavior is to be accepted, how-
ever, these classifications must be based on
the observable behavior of the animals in
natural settings with full appreciation of
intraspecific variability. Napier’s (1963) ar-
gument for “pseudobehavioral” classifica-
tions based on anatomy in the absence of
behavioral observations must be re’ected as
fJ
a misleading tautology. It follows rom this
reasoning that morphological diversity
among animals classified as vertical clingers
and leapers cannot be used to argue against
the validity cfthis behavioral c!ass. There is
certainly no a priori reason to expect that,
given the vagaries of evolutionary history,
all extant saltatory prosimians would have
arrived at identical biomechanical solutions
to the demands of an arboreal, saltatory way
of life. The existence of several distinct pat-
terns of femoral morphology among extant
prosimians does not support the morpholog-
ical component of the VCL h othesis.
T
Whether the behavioral category o vertical
clinging and leaping should remain, and to
which animals it should be ap lied, can be
E K
answered only by further be avioral re-
search. In any event, with their great diver-
sity of behavioral and morphological adapta-
tions, the prosimian primates will continue
to provide students of functional and evolu-
tionary biology with a wealth of research
opportunities.
 FEMORAL MORPHOLOI>Y AMONG PROSIMIANS 391
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