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A morphometric study of limb proportions in leaping prosimians

A morphometric study of limb proportions in leaping prosimians
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  AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 54:421-430 1981) A Morphometric Study of Limb Proportions in Leaping Prosim ans 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) ndriids, 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 bio- mechanical nature of the adaptation differs in different groups. The results, there- fore, 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 in- teractions 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 pro- portions 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 dimen- sions 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, primar- ily but not exclusively, in Old World primates. Received July 2. 1979; accepted September 8, 1980 0002-9483/81/5403-0421$03.00 981 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 over- all bodily proportions and such locomotor abilities among New World monkeys when grouped as general arboreal springers, ar- boreal climbers, and prehensile-tailed arm swingers. Other investigators have examined the pro- portions of prosimians as indicators of anatom- ical 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 re- viewed the morphological adaptations of leap- ing and constructed a group of prosimians which they call “vertical clingers and leapers.” This definition includes all known leaping spe- cies: indriids, bush-babies, and tarsiers, to- gether with some forms which, at 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 pro- simians 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 oined by Cartmill, 1972) hat 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) sepa- rate 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 mea- sures 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; n 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 pro- simians, but also many monkeys of both the New and Old Worlds that have in common only that they are generally adapted for quad- rupedal 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 spe- cies 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 adap- tations shown by Galago and Tarsius. 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 inves- tigations were undertaken in which as- sociations were drawn between the more de- tailed 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 locomo- tion not only between major groups of pro- simians, but also within genera between spe- cies 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, al- though still necessarily small, were considera- bly 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 be- havioral 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 at understanding the morphological correlates of leaping in the pro- simian 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 morpho- logical 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 leap- ing 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). n addition, however, it demonstrated a fourth morphological mode: The three cheirogaleines, C. mjor, C. medius, and Microcebus. The multivariate results also spoke to differ- ences within some of these groups. There was little evidence of a morphological spectrum within the indriids and the lemurs; each indi- vidual 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 spec- trum followed the association with the spec- trum of leaping behavior; in each case the forms that leaped least were nearest the most quad- rupedal 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, adapta- tion to extreme leaping should be evident throughout both limbs. Two of us (F.-K. Jouf- froy and the late J. Lessertisseur) have avail- able a suite of dimensions of the limbs taken from a wider range of prosimians and with somewhat larger sample sizes than in the ear- lier 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 investiga- tions attempt to examine and further elucidate include the following. Are the three morpho- logical 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 'Bx specimens of Cheirogaleus major and three of C Medius ing species also evident through examination of overall limb proportions? Are the morpho- logical 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 over- all 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 pro- simians 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 avail- able. 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 mea- sures 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 mea- surements) 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 treat- ment of the srcinal 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 infor- mation which they appeared to contain as judged from statistical tests. The lists of mea- surements and indices are provided in Tables 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, at least it could be confirmed that there were no univariate outliers. The princi- pal 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 informa- tion. 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 mea- surements 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) CN RA/ H+M) T/ F+P) M4N M/ RA+H) P/ F+T) C4N C/ RA+H) TW F+T) CUM1 M4/ RA+ H) T4/ F+T) C2/M2 TFUP T4/P 04/P om1 02m2 C4/ RA+H) O4/ F+T) C3N3 03IT3 HIF Humerusifemur) RAfI radiusitibia) M/P hand foot) CITR carpusitarsus) M4iT4 4th metatarsal/ 4th metacarpal) D41D4 4th finper/ 4th toe) total hindlimb) CN TRJP C4/M4 04m4 WMP total forelimb/ C 1 + Ml)/ C2+ M2) 0 +T1)/ 02 +T2) M4N T4P C1 +Ml)/ C4+M4) 01 T1)/ 04+T4) C4N 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 vari- ables. Second, the ratios were separated into suites of closely related dimensions to I) study dif- ferent anatomical regions and 2) assess the de- gree to which combinations of ratios were es- sential to the formation of the eventual result. Finally, using principal components analy- sis, an attempt was made to discover if any multivariate outliers existed. This showed that, indeed, two specimens were outlying. Re- examination of the srcinal 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; he mistake was cor- rected. The second specimen was found to in- clude data from a juvenile specimen of Zndri The result of including this specimen seemed to indicate that a small indri has proportions sim- ilar to Propithecus: It fell with Propithecus in the plot of the first two discriminant axes. If this were true, it might suggest that the sep- arations among the indriids were merely due to overall size. However, further examination of the generalised distances for these specimens showed clearly that the uvenile 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, how- ever, that if only it were possible to obtain sam- ples of differently aged individuals, interesting changes in proportions might be discovered for at least some of the species. These examples of the discovery and explanation of outliers mar- kedly 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 srcinal data to be described by a set of discrim- inant 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 infor- mation. 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 o 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 dif- ferences among the specimens, which is not unexpected. In comparison, the analyses of ra- tios produce much larger separations of the groups measured by between-group distance units. Moreover, these separations are consid- erably more complex in terms of the geometric
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