a morphometric study of limb proportions in leaping prosimians

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 54:421-430 (1981)

A Morphometric Study of Limb Proportions in Leaping -

Prosim ians CHARLES E. OXNARD, REBECCA GERMAN, FRANCOISE-K JOUFFROY, AND JACQUES LESSERTISSEUR Departments of Anatomy and Biology, and the Graduate School, University of Southern California, Museum of Comparative Zoology, Harvard University, and Laboratone d’AnatomiP Comparde, Museum National d’Histoire Naturelle, Pans

KEY WORDS morphometrics, Locomotion, Leaping

Prosimii, Limb proportions, Multivariate

ABSTRACT Study of individual limb proportions-most notably, for instance, of the intermembral index4istinguishes from most other primates those various prosimians capable of leaping. The present investigation analyzes 24 measures of limb proportions (taken by F.-K. Jouffroy and J. Lessertisseur) from 161 specimens representing 12 species of prosimians, using the multivariate statistical method of multiple discriminant analysis (carried out by R. German and C.E. Oxnard). The results indicate that there are three major gradients: 1) indriids, 2) cheirogaleines, and 3) galagines plus Tarsius, radiating from a fourth centrally located group of species, Lemur, Lepilemur, and Hapalemur.

It is likely that the morphometric relationships displayed here can be associated with behavioral (locomotor) parallels among these various forms. Though leaping is a most important adaptation among prosimians, it seems clear that it has evolved separately a number of times, and it seems at least likely that the biomechanical nature of the adaptation differs in different groups. The results, therefore, present certain new hypotheses about prosimian locomotion that can only be tested with further field and laboratory studies.

This study also emphasizes the fact that anatomical adaptation is complex. Though the analysis of each anatomical region separately provides a similar qualitative picture of the variation among genera, it is only in the analysis of all measures taken together that the complete pattern described above appears. Though no new variables have been added in that analysis, new information is ob- viously contained within the results. Since this information stems from the interactions of the variables, it must be due to associations between these anatomical areas.

Interest in the form and proportions of the entire body, and especially of the lengths of the limbs, has existed among students of land ver- tebrates for many years. Sometimes such proportions have merely been used as metrical de- scriptors of the shape of the body (the rationale, for instance, behind a great deal of such work, summarized and collated by Martin, 1957- 1966, as applied to man). But often, such studies have also been pointed at documenting differences in shape that seem to be related to functional differences, usually of locomotion.

Within the primates, although bodily dimensions are often taken to add to verbal and picto- rial systematic descriptions, interest in bodily form has also been aimed at associations with differences in locomotion. Thus Mollison (1910) separates various primates into Laufer, Springer, Kletterer, and Hangeler, and shows how these locomotor descriptions correlate with differences in overall bodily form, primarily but not exclusively, in Old World primates.

Received July 2. 1979; accepted September 8, 1980

0002-9483/81/5403-0421$03.00 0 1981 ALAN R. LISS, INC.

422 C.E. OXNARD, R. GERMAN, F.-K. JOUFFROY, AND J . LESSERTISSEUR

A more recent study by Erikson (1963) shows similar convincing associations between overall bodily proportions and such locomotor abilities among New World monkeys when grouped as general arboreal springers, arboreal climbers, and prehensile-tailed arm swingers.

Other investigators have examined the proportions of prosimians as indicators of anatomical adaptation for locomotion and many recent studies have been aimed at understanding the nature of morphological adaptation to leaping. Leaping in prosimians is so highly developed that some anatomically relevant aspects of their morphology are especially easy to iden- tify, for example, longer hindlimbs as compared with those of quadrupedal species. But the more detailed results of many of these studies have identified suites of characters which seem to describe a rather large number of leaping prosimians. Thus, Schultz in many early studies (reviewed in Schultz, 1969) notes many features of the markedly lengthened and strengthened lower limb elements that are used in leaping and shows that they are most evident in leaping species including sifakas, indris, bush-babies, and tarsiers. And, more re- cently, Napier and Walker (1967) have reviewed the morphological adaptations of leaping and constructed a group of prosimians which they call “vertical clingers and leapers.” This definition includes all known leaping species: indriids, bush-babies, and tarsiers, together with some forms which, a t that time, were less decisively known to be “vertical clingers and leapers”: Lepilemur and Hapalemur simus. This arrangement was noted by Napier and Walker (1967) as being tentative but is confirmed and further detailed by Walker (1974).

Yet, other investigators also studying prosimians do not group all these species in one locomotor adaptation but recognize two forms of adaptation to leaping. One of these includes Indri, Propithecus and Avahi which have an elongated thigh and a foot elongated in the metatarsus; the other includes Galago and Tarsius with long legs (as opposed to thighs) and with foot elongated in the tarsal region (Lessertisseur, 1970; Lessertisseur and Jouf- froy, 1973; Jouffroy and Gasc, 1974; Oxnard, 1973; Stern and Oxnard, 1973).

These authors all suggest modifications to the picture suggested by Napier and Walker (1967) on a number of grounds. First, each group of investigators reminds us that many very early studies (e.g., Morton, 1924; Volkov, 1903,1904; Mivart, 1867; and even earlier, Fit- zinger, reported by Brehm, 1868) draw at-

tention to the major differences, (from Fit- zinger), between “Brachytarsi”: Indri and Propithecus, and “Macrotarsi”: Microcebus, Galago, and Tarsius. Second, each group of workers also shows (and here they are joined by Cartmill, 1972) that the various measures used by Napier and Walker do not, in fact, differen- tiate a single group of “vertical leapers and clingers.” In this case, the evidence is mar- shalled most clearly in Stern and Oxnard (1973) who show that the main problem is not that these proportions either do (Napier and Walker, 1967) or do not (Cartmill, 1972) separate the leaping forms from the others, but rather, that any single proportion performs such a separation only partially.

The study of data like these requires a method that can view all the proportions at the same time yet not count identical information more than once. Such a method is, of course, the multivariate statistical approach, and Oxnard and colleagues have applied this approach to a variety of dimensions of different anatomical regions of prosimians, including some measures of the overall proportions of the limbs.

These studies (Oxnard, 1973; Stern and Ox- nard, 1973) do not confirm Napier and Walker’s (1967) grouping of all leaping prosimians into a single cluster. They show rather clearly that, whether the shoulder or pelvic girdles are stud- ied, or whether the proportions of the entire body are examined, those prosimians which are capable of extreme leaping are divided into at least two morphological modes. One of these includes Tarsius and Galago, the other all three indriid genera, Propithecus, Indri, and Avahi; in addition, these studies show that the nature of the morphological adaptation is such that each group lies morphometrically on op- posite sides of a centrally located set of species that includes not only a wide range of prosimians, but also many monkeys of both the New and Old Worlds that have in common only that they are generally adapted for quadrupedal locomotor habits with, of course, abilities for leaping (many primates leap quite well) but without the special propensities for leaping displayed in the particular genera named above.

In addition, the investigations of Oxnard and colleagues supply information about some species whose locomotion is incompletely known and whose anatomical adaptation seems equivocal. Microcebus and Cheirogaleus, what- ever their behavioral propensities for leaping, possess morphological adaptations of shoulder and hip, of upper and lower limb, and of overall bodily proportions-such that they differ from those of more quadrupedal animals and tend

MORF'HOMETRICS OF PROSIMIAN LIMB PROPORTIONS 423

somewhat towards the morphological adaptations shown by Galago and Tars ius . Lepilemur, in contrast, tends somewhat toward the morphological adaptation defining, Zndri, Propithecus, and Auahi. Lemur catta also leaps more than some other lemurs; its adaptation likewise tends a little towards the indriid morphological mode. Finally, the multivariate results are equivocal about the adaptation of Hapalemur; it seems to resemble the indriids somewhat in the shoulder, but tarsiers and bush-babies in the hip.

Expanding on these studies, further investigations were undertaken in which associations were drawn between the more detailed anatomy of the hip and thigh and the more complete behavioral information that is now available about these various species. The additional behavioral information stems from the investigations of a number of field workers in recent years (e.g., Charles Dominique, 1971, 1972, 1977; Kingdon, 1971; Bearder, 1974; Bearder and Doyle, 1974; Jouffroy and Lesser- tisseur, 1979; that can all be added to the prior work of Petter, 1962; Walker, 1967). They dem- onstrate that there are differences in locomotion not only between major groups of prosimians, but also within genera between species groups and even species. The more detailed treatment of the anatomical features of the animals resulted from improvements in the materials and methods. Thus sample sizes, although still necessarily small, were considerably greater than in the previous studies; almost every genus was represented. Where possible, genera were divided into species or species groups that accorded better with the new behavioral information about leaping (e.g., Galago crassicaudatus is known to leap less than G. Senegalensis, Cheirogaleus major less than C. medius). And finally, the study was specifically aimed a t understanding the morphological correlates of leaping in the prosimian hip and thigh.

The results of univariate analysis of both soft tissues and osteological dimensions in this study (McArdle, 1978) showed not only that leaping species (all of them) are different from nonleaping prosimians, but also that within the bush-babies, where there seems to be a gradation of leaping, an equivalent morphological spectrum exists. However, the different forms of leapers were not separated from one another; to this extent the results resembled those in the earlier descriptions of Napier and Walker (1967) although with much greater de- tail.

The subsequent multivariate statistical analysis of the data resulting from McArdle's

study was carried out by Oxnard et al., (1980). Although based only upon the hip and thigh, it separated two obvious groups of extreme leaping species (indriids on the one hand, and bush-babies plus tarsiers on the other) from the group of lemurs that, though well able to leap, are generally more quadrupedal. It thus con- firms the earlier studies of Oxnard (1973) and Stern and Oxnard (1973). In addition, however, it demonstrated a fourth morphological mode: The three cheirogaleines, C . m j o r , C. medius, and Microcebus.

The multivariate results also spoke to differences within some of these groups. There was little evidence of a morphological spectrum within the indriids and the lemurs; each individual genus displayed its own particular morphological characteristics within its group. However, within each of the other two groups, the new study demonstrated morphological spectra. In each case the morphological spectrum followed the association with the spectrum of leaping behavior; in each case the forms that leaped least were nearest the most quadrupedal species, the most extreme leapers were furthest away. Finally, the new study revealed two species generally intermediate between the more quadrupedal species and the leaping species; Lepilernur was intermediate between the lemurs and the indriids, Hapalemur was intermediate between the lemurs and each of the other two groups.

However, the hip and thigh are only one part of the leaping mechanism of these animals. Every bit as important are other particular anatomical regions such as the knee and foot, and other overall characteristics, such as bodily proportions.

This paper reports the results of further studies on limb proportions. For if the prior investigations of overall bodily proportions (Oxnard, 1973) hold up to any degree, adaptation to extreme leaping should be evident throughout both limbs. Two of us (F.-K. Jouf- froy and the late J. Lessertisseur) have available a suite of dimensions of the limbs taken from a wider range of prosimians and with somewhat larger sample sizes than in the earlier studies of Oxnard and colleagues. These data are analyzed here by two of us (R. German and C.E. Oxnard) using the multivariate statistical method in order to understand yet further the nature of the morphology of these prosimians.

The questions, then, which these investigations attempt to examine and further elucidate include the following. Are the three morphological modes of the hip and thigh in which more leaping prosimians differ from less leap-

424 C.E. OXNARD, R. GERMAN, F.-K. JOUFFROY, AND J. LESSERTISSEUR

TABLE 1 . Materials

Genus

Hapalemur Lemur Lepilemur Cheirogaleus Microcebus Avahi Indri Propithecus Galago Emticus Tarsius Total

No.

7 46

9 9"

15 6 6 7

39 9 8

161

' B x specimens of Cheirogaleus major and three of C. Medius.

ing species also evident through examination of overall limb proportions? Are the morphological spectra in the hip and thigh associated with increasing degrees of leaping in many leaping prosimians also found within overall limb proportions? Are those incipiently adapted genera identified by the study of the hip and thigh also present in the study of overall proportions of the limbs? To what degree does the study of overall limb proportions help increase our understanding of these various prosimian adaptations to leaping?

MATERIALS AND METHODS

Materials The data used in these analyses were derived

from measurements of 161 specimens of prosimians representing 11 genera. The detailed breakdown is shown in Table 1. Appreciable numbers of specimens were available for three genera; for the remaining eight, fewer than ten but never less than six specimens were available. However, small as these samples are, they are far higher than those in any prior study whether of our own (e.g., Ashton et al., 1975) or of others (e.g., Schultz, 1969).

Methods Dimensions

The present study is based solely upon measures taken from adult individuals as indicated in Table 1. Male and female subgroups were treated together as most of the samples are too small to study sex subgroups separately. All measurements were made uniformly by F.-K. Jouffroy and J. Lessertisseur according to the techniques outlined in their prior publications. Raw measurements of the lengths of bones are inadequate to describe differences in shape among species. However, the dimensionless numbers of Alexander (1971-ratios of measurements) may contain biomechanical or

functional information not found in the basic measurements from which they were derived. Thus the ratios upon which this study is based were obtained through the appropriate treatment of the original measurements. As it is difficult to determine which are the most useful ratios, a larger set was defined and several routine procedures used to reduce the number based upon the amount of independent information which they appeared to contain as judged from statistical tests. The lists of measurements and indices are provided in Tables 2 and 3.

Univariate analysis For each group of animals, the distributions

of the 26 measurements and the 51 ratios were examined. Although none of the samples are large enough to allow tests of normality to be undertaken, a t least it could be confirmed that there were no univariate outliers. The principal intergroup pattern of contrasts was also assessed, but the value of this procedure is min- imal as it is difficult to absorb and present such a large bulk of heavily overlapping information.

Multivariate analysis These data were then analysed using dis-

criminant functions as explained below. Be- cause of the possibility that certain problems with the data set might have influenced the results, a series of separate tests were carried out.

First, the data were analysed as raw measurements and then as ratios. This was done in order to make sure that the use of ratios did not produce an arrangement of genera that re- flected merely the overall sizes of the spec-

TABLE 2. Measurements

H RA M F T P MA MP C TR Ml,MZ,M3,M4 Cl,C2,C3,C4

Tl,TZ,T3,T4 01,02,03,04

Length of humerus Length of radius Total length of hand Length of femur Length of tibia Total length of foot Length of forelimb (H+RA+M) Length of hindlimb (f+T+P) Maximal length of carpus Maximum length of tarsus Lengths of metacarpals 1, 2 ,3 , and 4 Lengths of fingers 1, 2, 3, and 4

Lengths of metatarsals 1 , 2 , 3 , and 4 Lengths of toes 1 ,2 ,3 , and 4 (phalangeal

(phalangeal parts)

parts)

MORPHOMETRICS OF PROSIMLAN LIMB PROPORTIONS 425

TABLE 3. Indices derived from measures in Table 2

Forelimb Hindlimb Hand Foot Comparative

W(RA+M) F/(T+P) C N RA/(H+M) T/(F+P) M 4 N M/(RA+H) P/(F+T) C 4 N C/(RA+H) TW(F+T) CUM1 M4/(RA+ H) T4/(F+T) C2/M2

TFUP T4/P 04/P o m 1 02m2

C4/(RA+H) O4/(F+T) C 3 N 3 03IT3

HIF (Humerusifemur) RAfI (radiusitibia) M/P (hand foot) CITR (carpusitarsus) M4iT4 (4th metatarsal/

4th metacarpal) D41D4 (4th finper/ -

4th toe)

total hindlimb) C N TRJP C4/M4 04m4 W M P (total forelimb/

(C 1 + Ml)/(C2+ M2) (0 1 +T1)/(02 +T2)

M 4 N T4P (C1 +Ml)/(C4+M4) (01 +T1)/(04+T4) C 4 N 04/P (CZ+MZ)/(C3+M3) (02+T2)/(03+T3)

(CZ+MZ)/(C4+M4) (02+T2)/(04+T4) (C3+M3)/(C4+M4) (03+T3)/(04=T4)

(Cl+Ml)/(C3+M3) (01+T1)/(03+T3)

imens. As no precise measure of overall size (such as trunk length, body weight, or oth- erwise) was available, it was not possible to perform regression analyses against such variables.

Second, the ratios were separated into suites of closely related dimensions to I) study different anatomical regions and 2) assess the degree to which combinations of ratios were es- sential to the formation of the eventual result.

Finally, using principal components analysis, an attempt was made to discover if any multivariate outliers existed. This showed that, indeed, two specimens were outlying. Re- examination of the original data revealed that one of these was due to a mistake in computer coding-a specimen of Galago had been mis- takenly coded as Euoticus; the mistake was cor- rected. The second specimen was found to include data from a juvenile specimen of Zndri. The result of including this specimen seemed to indicate that a small indri has proportions similar to Propithecus: It fell with Propithecus in the plot of the first two discriminant axes. If this were true, it might suggest that the separations among the indriids were merely due to overall size. However, further examination of the generalised distances for these specimens showed clearly that the juvenile indri was some seven distance units away from Propithecus. The net outcome, therefore, was the rejection of this particular specimen of Indri on the basis that it was not adult. The result suggests, however, that if only it were possible to obtain samples of differently aged individuals, interesting changes in proportions might be discovered for a t least some of the species. These examples of the discovery and explanation of outliers markedly increases intuitive trust in the power of the method.

Multivariate technique In these studies, the variation of the group

structure in the data is of greater interest than either the total variation among the specimens taken as a single universe, or the variation of the specimens within each individual group. Assuming that the groups defined are natural taxonomic units (Oxnard, 1978a) and this is highly likely given their separation by taxon- omists, the multivariate technique used must take into account this a-priori-grouped nature of the data. Discriminant analysis is the logical method to use in such a case. It allows the original data to be described by a set of discriminant functions derived one at a time, each one presenting the largest part of the information in the data that is uncorrelated with what has already been presented. Statistical tests allow determination of how many of these functions are providing important discriminating information. Equalization of variances allows scal- ing in standard deviation units to be applied in all directions and to all groups. The method has been well described in many texts (e.g., Gnanadesikan, 1977).

RESULTS

Analysis of raw measurements The analysis of measurements provides a pic-

ture that displays most of the separations among genera within the first discriminant axis (94% of the information). This pattern of contrast is highly correlated with size differences among the specimens, which is not unexpected. In comparison, the analyses of ratios produce much larger separations of the groups measured by between-group distance units. Moreover, these separations are considerably more complex in terms of the geometric

PROSIMIAN FOOT II

7.0

3.5

0.0

- 3.5

- 7.0

C heirogoleur medius 0

0 M i c r o c e b u r

C . major

Euoticur Avahi

0 l e p i l e m u r Torriur 0

Hapalemur O .

0 lemur

Galago

Propi fhecur

l n d r i

5 0 OD -50 I

Fig. 1. Separation of genera produced by discriminant axes 1 and 2 of analysis of suite of foot indices. Scale is in standard deviation units; the analysis is performed with group variances equalized so that a single scale is proper for all groups and all axes.

TABLE 4. Eight analyses and their relative significance ~ ~~ ~ ~ ~~

Axis 1 Axis 2 Axis 3 Axis 4

Analysis % cc % cc % cc % cc * Foot 78 96 16 84 43 *

Hand 42 81 32 77 12 54 Forelimb 61 88 25 73 11 56 * Hindlimb 55 94 40 82 3 54 * Comparative

indices 71 90 22 77 3 34 * Forelimb plus

hindlimb 44 94 33 92 10 81 3 61 Forelimb plus

hindlimb plus comparative indices 48 96 28 94 13 86 5 73

All indices 47 98 24 94 13 92 7 88

Values are Percent of total variance in axis and squared canonical correlation (CC). *Less than 2%.

*

arrangements of the groups. Thus, the results The first four analyses included, separately, discussed in this paper are from analyses of the hand, foot, forelimb, and hindlimb. A fifth ratios. included a study of indices comparing the fore-

limb with the hindlimb, and the hand with the foot. The remaining three analyses were in- Analysis of ratios

Eight analyses of ratios were carried out on creasingly larger combinations of the previous the subsets of variables indicated in Table 3. subsets: The hindlimb and forelimb indices

TABLE 5. Values for genera in most significant discriminant axes of study of all indices

Genera Axis 1 Axis 2 Axis 3 Axis 4

Hapalemur Lemur Lepilemur Cheimgaleus C. medius Microcebus Auahi Propithecus Indri Galago Euoticus Tarsius

major

3.18 3.04 2.10 0.10 0.61

-2.00 12.71 10.32 15.31 -8.04 -6.14 -3.79

-2.06 -0.97 -0.43 -6.96 -7.07

-10.63 3.55 4.00 6.94 3.61 1.94 4.45

4.67 1.82 3.61 0.48

-4.20 -4.97 -3.48 -1.38 -6.32

0.06 -1.57 -5.72

-0.99 1.29 0.48 0.17 0.56

-1.33 -1.30 -4.19 -3.25 -1.79 -0.50

9.52

II

-10

- 5

0

5

1I

lndriidr

PROSIMIAN OVERALL LIMB INDICES

Gologinor + Tarsius

i a b 0 -b I

Fig. 2. Separation of groups of genera produced by discriminant axes 1 and 2 of analysis of the suite of all indices of both limbs. The individual genera were entered into the analysis; they emerged grouped as shown here. Scale in standard deviation units as in Figure 1.

taken together; then the hindlimb, the forelimb, and the group of indices comparing fore with hindlimb and hand with foot; and finally, all indices combined.

The first four analyses produce a somewhat similar result (hence, a single plot, Fig. 1, suffices to display it). Two significant axes alone contained the great majority of the variance (Table 4). In each case, but to pro- gressively greater degrees in proceeding from studies of the hand, through the forelimb, through the hindlimb, to the foot, the indriids are clearly separated from the mass of other prosimian genera; the bush-babies and tarsiers are scarcely separated in the studies of the

hand but become increasingly so as one pro- ceeds through the series of studies.

A strikingly more complex pattern emerges from the remaining four analyses even though they are only combinations of the measurements used in the first five. This is most clearly seen in the analysis of the entire suite of indices (Table 4 and 5, and Figs. 2 , 3 and 4). The first axis (47% of the variance) places indriids at one end of the separation and cheirogaleines, bush-babies, tarsiers, and needle clawed bush-babies a t the other. The second axis (27% of the variance) discriminates between the aforementioned groups and the cheirogaleines. The third axis (only 13% of the variance but all of

428

I I

-1 0

- 5

0

5

C.E. OXNARD, R. GERMAN, F.-K. JOUFFROY, AND J. LESSERTISSEUR


Microcabus

Cheirogaleus mediur 0

0 C. major

Hapalemur 0

Tarsius 0

lndr i

Euoticus 0

0 Galago

18 12 6 0 -6 I

Fig. 3. Disposition of each named genus within each group shown in Figure 2. Again, individual genera were entered into the analysis; such grouping as has emerged results from the morphometric relationships of the genera. Scale in standard deviation units as in Figure 1.

it involved in the separations of only two genera) distinguishes Hapalemur and Lepilemur from the genuslemur. The fourth axis (an even lesser portion, 7%, of the variance but all con- centrated in a single genus) separates Tarsius by some nine standard deviation units from the various bush-babies.

The remaining analyses produce qualitatively similar pictures but with lesser separations and lower canonical correlations.

DISCUSSION

Though study of the limb proportions in a univariate manner is unable to do more than separate the most extreme leaping species from those that are less extreme, the first five multivariate analyses-the studies of the four dis- crete anatomical regions and the ratios comparing upper lower limb elements-produce more complex results. Two significant axes dis-

criminate among the three morphological groups: Extreme indriid leapers, extreme galagine-plus-tarsier leapers, and less extreme lemur leapers, as identified by Oxnard (1973) and Stern and Oxnard (1973). In some anatomical regions these separations are of lesser degree (the forelimb, for instance); in others they are considerably greater (the foot, for example; see Fig. 1).

The results of the final three analyses, however, differ qualitatively from the preceding. Although they include no new measurements, they produce an even more complex picture. They show four widely separated clusters of species described by three markedly significant axes: The indriids, the combined group of bush-babies and tarsiers, the cheirogaleines, and the lemurines (Lemur itself, Hapalemur and Lepilemur, Figs. 2 ,3 and 4). These clusters of groups are the same as those observed by

MORPHOMETRICS OF PROSIMIAN LIMB PROPORTIONS


-10 -.

-5 - .

0 -

5 -

429

Avahi + + + + * +* **

0 0

Cheirogofeus medius 4 4 0 5 c. m a j o r

0 H o p a l e m u r k A

A a * Euoticus

A Lemur

* Propi fhecus * c Torsius

b O 0 %% 0003

Gofogo

18 12 b b -6 I

Fig. 4. Disposition of each specimen for each genus shown in Figure 2. Scale in standard deviation units.

Oxnard et al. (1980) in their study of the dimensions of the hip and thigh and which they suggest are associated with different anatomical modes for leaping.

That the same morphological modes for different degrees and forms of leaping observed in the studies of the hip and thigh, also exist when less detailed measures of far wider anatomical localisation are examined is not unreasonable. Although functional impacts of leaping ought to be clearly observable upon the structure of the hip and thigh, they should also affect all other regions of the body. Locomotion is not an independent operation of one anatomical region, but a function of the entire body.

Additional information about specific genera is also available from these studies. Hapalemur andlepilemur, genera for which some evidence exists about incipient adaptation for leaping (e.g., Napier and Walker, 1967) are specifically separated here from the genusLemur by higher

discriminant axes suggesting that they share some anatomical elements distinct from those of Lemur; this may imply that they also share yet another pattern of leaping that distinguishes them from Lemur. This can only be settled by further behavioral and anatomical studies.

Additional information also demonstrates that Tarsius, though clearly allied morphometrically with the bush-babies, is uniquely separated from them. Generally similar biomechanical leaping for Tarsius and the bush- babies may thus be suggested as having evolved from independent morphological bases, i.e., in animals that are taxonomically quite separate (see Oxnard, 197813).

It certainly seems, then, that overall limb proportions-though individually rather non- specific measures of form that produce little separation among prosimians-reveal, when examined using multivariate techniques, re-

lationships among these genera that seem to speak strongly to functional adaptation and perhaps more than a little to their taxonomic classification.

A final most interesting point that arises from these results is why the three final analyses produce more complex results than the first five. The ratios which weigh heavily into the first five analyses also weigh heavily into the latter three. And plotting the axes of (say) the forelimb analysis alone against the axes of the hindlimb analysis does not produce the more complex result of analysing both regions together. The new information in the mm-e complex result resides in the effect of combining the information in these distinct anatomical regions as well as in the effect of adding them together as separate entities. Thus, some important differences in the shapes of these animals are a function of the interactions of their parts as well as the sum of the individual parts.

ACKNOWLEDGMENTS

The data were obtained by F.-K. Jouffroy and Jacques Lessertisseur of the Museum National #Histoire Naturelle, Paris. The multivariate statistical analyses were carried out primarily in the Department of Anatomy, University of Chicago, by Rebecca German and Charles Ox- nard, and by Rebecca German a t the Depart- ment of Geology, University of Rochester. We thank Mrs. Marsha Greaves, Miss Joan Hives, Mrs. Eleanor Craycraft, and Messrs. Hugh and Guy Oxnard for help with secretarial, drafting, and computational tasks. The work is sup- ported by NSF grants GS 30504, DEB 81939, and DEB 24366 to C.E. Oxnard, by C.N.R.S. grant 031994 to F.-K. Jouffroy, by Museum Na- tional #Histoire Naturelle funds to F.-K. Jouf- froy and Jacques Lessertisseur, and by Univer- sity of Southern California Associates Funds to Charles Oxnard. With deep regret, we record the death of Jacques Lessertisseur near the end of the investigation.

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Bearder, SK (1974) Aspects of the ecology and behavior of the thick-tailed bushbaby Galago crassicaudatus. Ph. D. Thesis. University of the Witzwatersrand, Johannesburg.

Bearder, SK, and Doyle, GA (1974) Ecology of bushbabies Galago senegalensis and Galago crassicaudatus, with some notes on their behaviour in the field. In: Prosimian Biology. RD Martin, GA Doyle, and AC Walker, eds. Duckworth, London.

Brehm, AE (1868) La Vie des Animaux Illustree, Les Mam- misres. Volume 1. Bailliere et fils, Paris, pp 130 and 140.

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a morphometric study of limb proportions in leaping prosimians

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