The Functional Adaptations of Primate Molar Teeth RICHARD F. KAY Department of A n a t o m y , Duke University Medical Center, D u r h a m , North Carolina

KEY W O R D S Molar structure Mastication . Primates.

. Teeth . Feeding

adaptations

ABSTRACT Measurements were taken on the upper and lower molars of 37 species of primates and one tupaiid to assess the relative importance of shearing, crushing and grinding features. Significant correlations were found between pairs of allometrically standardized dimensions which measure the same molar function (shearing, crushing, or grinding). Correlations between pairs of dimensions which do not measure the same finction are not significant. Second molar adaptations for shearing, crushing, and grinding, as well as the length of the second lower molar, and the total surface of the post-canine dentition are negatively allometric with respect to metabolic rate. Species which take different proportions of fruit, leaves, and insects in their diets have different molar structure. Frugivores have small teeth for their adult body size with poorly developed shearing, crushing, and grinding features on their molars. By contrast, leaf-eating species tend to have large teeth for their adult body size with well developed shearing, crushing, and grinding. The second molars of insectivorous species were found to parallel closely those of leafeating species. The two groups are clearly distinguishable from the former on the basis of body size alone: the smallest living primate leaf-eater is on order of magnitude larger than the largest living primate insectivore.

The observation that teeth are fitted for breaking up food has been commonplace among comparative mammalian anatomists since ancient times. In the third century B.C. Aristotle quoted an example of the views of Empedokles: “. . . for teeth should come up of necessity-the front teeth sharp, fitted for tearing, the molars broad and useful for grinding down the food . . .” (Physica). Aristotle recognized comparative differences in tooth structure: “. . . some animals are saw-toothed, such as the lion, the pard, and the dog; and some have teeth that do not interlock but have flat opposing crowns as the horse and the ox . . .” (Historica Animalium). More refined observations on dental mechanics were not made until the eighteenth century, when John Hunter [1771, 1861 (posthumous)] noted that the teeth of mammals are used to catch, collect and prepare food for digestion, that chewing is a dynamic process, and that the variety of ways in which food acquisition and preparation occur reflect the physical nature of the AM. J. PHYS.ANTHROP.,43: 195-216.

materials on which each animal feeds. He distinguished the dentitions and jaw movements of those animals which feed on flesh from those which eat grain and concluded that the human dendition is fitted for the conversion of both animal and vegetable substances into “blood.” Cuvier (1863) noted that the molars of herbivorous mammals are not compact in structure, the enamel is infolded, and the tooth roots are continuously growing. He characterized the molars of carnivores as smooth and compact in structure, not infolded, and limited in growth as they are worn down to sumps with age. Ryder (1878, 1879) advanced the notion that a more transverse and less vertical jaw movement in chewing increases the time of tooth contact. He tied increases in transverse movement to increases in enamel folding, ridging, and cresting, advantageous for mammals eating fibrous plant foods. Cope’s (1883)exposition of his “tritubercular theory” included a clear recognition 195

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RICHARD F. KAY

that mammalian tooth crests and surfaces are adapted for shearing and crushing food. Cope's student, H. F. Osborn (1895), attempted to explain how mammalian dentitions evolved from simple conical reptilian teeth. The acquisition of a series of alternating reversed V-shaped crests between upper and lower molars was seen as a more efficient shearing mechanism than reptilian shearing involving cusps in a line. Osborn further noted that the evolution of lower molar basins to receive upper molar cusps was related to the appearance of crushing functions in mammalian chewing. The concept that the evolution of tooth shape involves improvement of mechanical efficiency for chewing particular kinds of foods was applied to primate molar teeth by Gregory ('22). He reviewed the evolution of the human dentition from the primitive tribosphenic molar structure. He inferred that tooth changes involved an adaptive response to dietary changes. Simpson ('33) extended and elaborated the work of Cope, Osborn, Gregory and others on the functional anatomy of mammalian molar teeth. He recognized three categories of jaw movement among mammals: (1) simple vertical opposition where the teeth come to rest after contact; (2) nearly vertical movements with slight horizontal components; and (3) chiefly horizontal motion, with the teeth sliding across each other in prolonged contact. He correlated these movements with four general principles of molar occlusion: alternation between upper and lower tooth elements; opposition, or crushing; shearing either by movement of crests across each other or by the movement of a crest across a surface; and grinding by cusps or cusp rows being dragged across grooves or by opposition of crested surfaces. Changes in dentitions and jaw movements could maximize one or more of these functions depending on their selective advantages of these designs for a particular food specialization. Following the lead of Simpson ('33) and Crompton and Sita-Lumsden ('70), Kay and Hiiemae ('74a) offered refined definitions of shearing, crushing and grinding and identified design features on the molars which relate to these functions. The relative contributions of these features to tooth design were seen as indicators of

their relative importance for mastication. The authors also showed how jaw movements and tooth structure have changed in the evolution of primates and inferred that various changes have also occurred in the kinds of foods prepared. This paper seeks to extend and refine the proposition that foods with different physical properties select for different optimum molar mechanical designs (shearing, crushing, grinding). Several selective influences on tooth shape may be distinguished: 1. Body size. Small animals have higher energy requirements per unit body size than large ones. An animal which weighs 5 grams consumes daily more than its total body weight in food whereas one which weighs 50,000 grams consumes only a small fraction of its body weight in food (Kleiber, '61). In other words, small animals have proportionately more food to prepare than large ones. Thus, two animals of different size which are adapted to eat the same foods may have quite different tooth shapes because of proportionate differences in the amount of food preparation needed to meet their energy needs. 2. Energy content offood. Placental mammals of the same size have roughly the same basal metabolism and therefore the same energy requirements (Kleiber, '61). The energy content of food influences the total amount of food which has to be prepared per unit time and should influence tooth designs for mechanical efficiency and for wear resistance. 3. Food consistency. The physical properties of foods selectively affect the shape of food preparation designs. The approach advocated here is to segregate and analyse separately the three factors, body size, energy needs, and food consistency and their influence on the shape of primate molars. Tooth shape is also affected by the heritage of the animal (Simpson, '53). Animals of different heritage which undergo selection favoring convergence on a common feeding adaptation may adapt themselves in different ways in response to this selection. The molars of living primates and tupaiids have the same detailed pattern of tooth contacts during chewing (Kay and Hiiemae, '74a,b). In addition the jaw movements are similar during preparation of food in tupaiids and primates with widely disparate molar shapes (Hiiemae and Kay,

PRIMATE MOLAR ADAPTATIONS

’72, ’73). Therefore, because of the similarities in molar contacts and jaw movements, heritage features have a minimal contribution to the differences between species. The exception to this generalization is the presence of “bilophodont” molars in Old World monkeys. Consideration of the adaptive significance of bilophodonty has been deferred until completion of a study of the jaw movements in a representative of this family. Such a study is currently nearing completion.

197

tion on lower second molars is the sum of the estimated areas of the anteromedial surfaces of the hypoconid and protoconid. When the contact area is expanded onto the posterior surface of the trigonid, this was included. (5) Phase I traverse: the distance of the second lower molar hypoconid traverse across the second upper molar in Phase I of mastication is estimated from the distance between the junction of crests running posteriorly from the paracone and anteriorly from the metacone, and the deepest point of the trigone basin on the MATERIALS A N D METHODS upper second molar. (6) Phase 11 traverse: One hundred and ninety-eight osteolog- The traverse of the second lower molar ical specimens from the American Museum hypoconid across its corresponding upper of Natural History, the Yale Peabody Mu- molar in Phase I1 is estimated from the seum and the Museum of Comparative distance between the deepest points of the Zoology, Harvard University, including rep- trigone basin of the upper second molar resentatives of tupaiids and every family and the edge of the medial facing surface of living primates except Cercopithecidae of the protocone along the path of Phase I1 were examined in this study. Since osteo- hypoconid movement. logical specimens rarely carry such assoLinear measurements were made in milciated information, the body-mass estimates limeters with a Helios dial caliper, or when required for allometric studies were taken specimens were too small to be measured from the literature (table 1). When sexual accurately in this manner, with a calidimorphism was considerable the sample brated reticle mounted on a binocular was segregated by sex and separate body microscope. Surface area estimates were mass figures were used for males and fe- made by orienting each crushing surface males. Five tooth measurements were taken parallel to the plane of focus of the microon second upper and lower molars and scope, and drawing its outline using a first molars only of callitrichids (because camera lucida. The area within each outof the reduced condition of their second line was measured with a polar planimeter; molars). All dimensions are illustrated in the surface areas for each plane on the figure 1 and their mean values for each tooth were summed, and corrected for taxon are listed in table 1. magnification. Descriptions of the tooth measurements In addition to simple univariate and biare as follows (for more details, see Kay, variate statistics, two variations of princi’73): (1) The maximum length of the sec- pal components analysis were used. Prinond lower molar in the long axis of the cipal components analysis is a technique tooth row is an estimate of post-canine by which a number of variables measured tooth size. A correction was made for speci- on a number of individuals are linearly mens with heavy interstitial wear, on the transformed to produce a set of new varibasis of the shape of unworn specimens. ables independent of each other (ortho(2) Length of the cristid obligua of the gonal) such that each of the new variables lower second molar. The cristid obliqua is (a principal component) accounts succesa major crest on the lower molars of Tupaia sively for as much as possible of the total and all primates used in this study. ( 3 ) variability of the system. Usually the first Projective crown height of the lower second three components soak up enough of the molar, the distance between the tip of the total variability to allow a relatively undishypoconid and the ventral-most extent of torted visualization of the relationships the cemento-enamel junction at its base. between individuals. The nature of the (4) Area of crushing and grinding surface: first and successive principal components the maximum area of potential tooth con- can be deduced from examination of the tact between upper and lower teeth at the linear transformations (Wahlstedt and beginning of the second phase of mastica- Davis, ’68). Principal components analysis

198

RICHARD F. KAY TABLE 1

Means of tooth measurements i n millimeters or square millimeters taken f r o m dental specimens of extant species Species

Tupaia glis (1) Lemur catta (7) Lemur rubriventer (1) Lemurfulvus (5) Lemur variegatus (5) Hapalemur griseus (5) Lepilemur mustelinus (6) Cheirogaleus major (2) Microcebus murinus (7) Phaner furcifer (1) Propithecus verreauxi (6) Avahi laniger (3) Indri indri ( 3) Daubentonia madagascariensis (1) Loris tardigradus (4) Arctocebus calabarensis (1) Perodicticus potto (5) Galago crassicaudatus (6) Galago alleni (2) Galago elegantulus (5) Galago demidovii (5) Tarsius spectrum (8) Callithrixjacchus (5) Saguinus geoflroyi (8) Aotus trivirgatus (8) Pithecia pithecia (7) Chiropotes satanas (4) Alouatta villosa (males) (3) Alouagta villosa (females) (3) Cebus capucinus (males) (4) Cebus capucinus (females) (4) Saimiri sciureus (5) Ateles geoffroyi (8) Hylobates klossi (7) Symphalangus syndactylus (10) Pongo pygmaeus (males) (4) Pongo pygmaeus (females) (4) Pan paniscus (3) Pan troglodytes (males) (5) Pan troglodytes (females) (5) Gorilla gorilla gorilla (males) (6) Gorilla gorilla gorilla (females) (5)

LMz

C.O.

C.H.

PI

PI1

S.A.

3.2 5.2 5.8 5.9 6.6 4.5 4.0 3.6 1.8 2.7 6.5 3.7 7.2 3.8 2.6 3.6 3.7 3.8 2.8 2.5 1.7 2.4 2.2 2.6 3.2 3.8 3.7 7.8 7.5 4.2 4.0 2.6 5.3 5.6 8.7 15.2 12.8 9.0 11.3 10.4 17.6 14.5

1.3 1.8 1.9 2.1 1.8 1.6 1.3 0.9 0.8 1.0 2.4 1.6 2.6 1.1 1.3 1.6 1.0 1.5 1.2 1 .o 0.7 0.9 0.7 0.9 1 .o 0.8 0.9 2.9 2.8 1 .o 0.9 1 .o 1.2 1.2 2.0 2.7 2.5 2.2 2.1 2.0 4.1 3.4

1.5 2.3 2.8 2.8 3.4 2.6 1.9 1.5 0.9 1.5 3.3 1.7 3.6 1.2 1.7 1.6 1.8 2.1 1.6 1.5 1.1 1.5 1.3 1.6 1.7 1.6 1.5 3.9 4.0 2.4 2.1 1.5 3.0 3.2 4.3 7.6 6.6 5.1 6.7 5.8 9.7 7.0

1.4 1.6 1.4 1.3 1.6 1.0 1.1 1 .o 0.6 0.9 2.3 1.8 2.4 1.3 0.8 1.2 1 .o 1.1 1.0 0.9 0.7 0.9 0.7 0.7 0.9 1 .o 1 .o 3.1 3.1 1.1 0.9 0.8 1.5 1.6 1.9 3.9 3.7 2.3 2.7 2.5 4.3 3.6

1.2 1.9 2.4 2.3 2.6 1.9 1.3 1.3 0.7 1.1 2.1 1.6 2.5 1.3 0.8 1.0 1.4 1.2 1 .o 0.9 0.7 0.9 0.8 0.9 1.6 1.8 1.9 2.9 3.3 1.6 1.7 1 .o 2.4 2.4 3.2 6.6 6.0 31.1 43.1 40.2 6.6 5.2

2.1 4.1 6.5 6.4 8.5 4.0 2.0 1.9 0.8 1.1 8.4 3.6 13.2 6.6 1.4 2.5 3.1 3.6 2.1 1.7 1.2 1.1 0.8 1.1 3.1 6.2 7.3 20.0 18.0 7.0 6.3 2.0 8.5 10.4 18.3 98.3 68.4 4.7 5.0 4.3 100.4 71.0

Body mass

160 2,300 2.400 2,400 4,000 2,600 800 450 60 440 3,800 1,000 6,200 2,100 200 200 1,200 1,100 (260) 300 60 115 220 550 1,000 1,050 2,950 7,400 6,350 3,540 2,640 670 7,800 5,300 10,100 78,000 36,000 35,000 45,000 36,000 167,000 123,000

The number in parenthesis to the right of the species is the sample size. LMz, length of Mz; C.O., length of cristid obliqua of Mz; C.H., MZ crown height at hypoconid; PI, Phase I hypoconid traverse across MZ; PII, Phase I1 h y p o conid traverse across M2; S.A., surface area Mz crushing. The measurements are defined in the text. The last column lists the approximate adult body mass in grams of each taxon. For a detailed bibliography of body masses of primate species refer to Kay ('73). The body mass estimate for Galago alleni is probably too small for the dental specimens used. See Note added in proof.

usually consists of a series of operations performed on a variance-covariance matrix of the original variables. However, a second approach can also be utilized in which the same operations are performed on a transformed association matrix based on relationships between individuals rather than between variables. This variant of principal components analysis is commonly referred to as principal coordinates analysis. (For a mathematical treatment, see

Blackith and Reyment, '71). Two computer programs were used: a principal components analysis program from the Statistical Package for Social Sciences, and a principal coordinates analysis program presented in Blackith and Reyment ('71), and modified for compatibility with the Yale University Computer Center by Michael Zwell, Peter Dodson and the author. Dimensions were transformed for parts of the analysis to eliminate the effects of body size as fol-

199

PRIMATE MOLAR ADAPTATIONS

surement and the difference between them is expressed in the form:

LENGTH I

[A )

I

“percentage difference” =

M2

CRlSTlD OBLIQUA HY POCONID

CROWN HEIGHT

PHASE I

I

100 (observed-expected)

expected

(5) Animal A is returned to the data set. Animal B is selected and steps 2 through 4 are repeated. A complete data set is composed of 6 tooth measurements for each animal, each measurement standarized with respect to the tooth measurement predicted for an “average” primate of its body mass. In other words, we can now say that animal A has X% more of character Y than would be expected for an average primate of its body weight. “Average” in this sense refers to the complete data set used in this study. RESULTS

PARACONE

TRIGONE

Fig. 1 Occlusal (A) and lateral (B) aspects of the lower second molar and occlusal aspect (C) of the upper second molar of Pelycodus ralstoni; Early Eocene, Big Horn Basin, Wyoming, illustrating the dimensions used in this study and the dental anatomy discussed. Stippled areas on the upper and lower molars are areas where food is crushed at the termination of the first phase of the power stroke; the heavy arrows in C indicate the direction of the hypoconid traverse during the phases of the power stroke. For a more detailed discussion of dental anatomy see Kay and Hiiemae (’74).

lows: (1) Dimensions were converted into natural logarithms. (2) Species A was eliminated from the data set and regressions were calculated between the log, cube root of body mass (the independent variable) and the loge of each tooth measurement using the taxa remaining in the data set. (3) The value of each tooth measurement for animal A was estimated from that animal’s body mass using the regression equations from step 2, the “predicted” tooth measurement for an “average” primate with the body mass of animal A. (4) The “predicted” tooth measurement for animal A is converted to a real number and compared with the observed tooth mea-

A. Leuels of integration in primate molars The measurements used for this study assume five basic factors in molar design: (1) Body size and molar size. The cube root of the mean adult body weight of each species is a metabolically relevant measure of body size; the length of a lower molar is a measure of the size of the molar tooth battery. ( 2 ) Resistance to tooth wear. The height of the hypoconid cusps is a measure of cusp height. High crowns and cusps should resist tooth wear for a longer period of time before wearing out. The longevity factor should be important in all aspects of tooth function. (3) Measures of shearing function. Cristid obliqua length expresses the amount of shearing in the molar battery. This shearing blade is always one of the most well developed on the entire dentition. The length of the traverse of the lower molar hypoconid cusp across the upper molar in Phase I indirectly measures shearing function because shearing occurs in this phase of the power stroke. (4) Measures of crushing function. Crushing was estimated from the size of those surfaces in the lower basins molar which contact at the termination of Phase I of mastication. The length of the Phase I traverse of the hypoconid mentioned above is a second, indirect, measure of this function (crushing occurs at the termination of this phase). ( 5 ) Measures of grinding function. The same surfaces which function in crushing

200

RICHARD F. KAY

less of functional differences. That this factor masks correlations due to functional interactions is illustrated by the sizes of the partial correlations between log, cube root of body mass and pairs of tooth measurements used. Six of the partial correlations of tooth measures and body size are significant at the 0.999 confidence level, two are significant at the 0.99 confidence level and one at the 0.95 confidence level. Only the partial correlation between the Phase I1 traverse of the hypoconid and crushinggrinding tooth surfaces is signficant irrespective of body size (partial correlation of body mass and this pair of tooth measurements is 0.18, which is not significant even at the 0.90 confidence level). Transforming tooth measurements into “percentage difference” form before coefficients of correlation are estimated eliminates the contribution of body size to the correlation between pairs of variables. This technique measures the positive or negative deviation of tooth measurements of a species from that predicted by regressions between body size and each tooth measurement. Correlations between pairs of log, percentage difference tooth measurements are presented in table 3 . Pairs of tooth measurements can be linked through common factors (fig. 2). For example, the

at the termination of Phase I serve as grinding surfaces in Phase 11. The length of the traverse of the lower molar hypoconid across the surface of the upper molar is an indirect expression of grinding function, which is completely restricted to this phase of the power stroke. Figure 2 summarizes the relationship between tooth measures and molar tooth function. Coefficients of correlation (r) were calculated for pairs of estimates of the means of pooled tooth measurements for 42 taxa. This is a fundamentally different approach from the one usually advocated where correlations are calculated between pairs of estimates of means aqd standard deviations of measurements within each species (Gould and Garwood, ’69; Olson and Miller, ’58). Thus, correlations were calculated between measurements for all species rather than between measurements in each species. In this way, the relationship between tooth shape and function can be analyzed for a large natural group rather than between pairs of species. Calculated correlations are listed in table 2 between the natural logarithms of all tooth measurements. Overall body size has a significant effect on the correlations listed in the table. ln general, the teeth of large species are larger than the teeth of small ones regard-

TABLE 2

Correlations between the loge of unstandardized tooth measurements ranked according to their intensity, and the partial correlation coefficients between these variables and the loge of the cube root of body weight Variable pair

r

S.A. X PI1 C.H. X PI1 S.A. X C.H. S.A. X PI PI X C.H. PI x C.O. PI1 x PI C.H. X C.O. PI1 x C.O. C.O. X S.A. Body mass

Body mass LM2

Partial correlation between variable pair and body weight

0.971 0.954 0.937 0.919 0.916 0.916 0.915 0.873 0.818 0.809

0.184 0.603 0.442 0.583 0.55 3

0.773 0.613 0.62 3 0.442 0.31 1

LMz

C.O.

C.H.

PI

PI1

S.A.

1 .o

0.956 1 .o

0.769 0.887

0.932 0.972

0.876 0.944

0.962 0.977

0.966 0.967

1 , 6 0 . 0 5 ; 2 , S 0.01; 3 , 60.001; 4 , n, not significant. At the bottom are listed the correlations between loge body mass and loge of all other measurements; and between log, MI tooth length and log, of all other measurements. Body mass and tooth length were considered as direct estimates of body size. Symbols are the same as in table 1.

PRIMATE MOLAR ADAPTATIONS

20 1

TABLE 3

The correlations between pairs of loge of standardized tooth measurements which are associated w i t h a common functional factor, shearing, crushing and grinding (see text and f i g . 2 for explanation). Listed in parenthesis after each pair is the correlation rank in the unstundardized data set. Asterisk indicates that measurements are significantly greater than zero at the 99% confidence level r

Rank for this data set

Shearing C.O. x PI (6) (2.0. X C.H. (8) C.H. X PI (5)

0.755" 0.661 0.567'

Crushing S.A. X PI (4) S.A.X PI1 (1) C.H. X PI (5) C.H. X PI1 (2) C.H. X S.A. (3) PI1 x PI (7)

0.625" 0.578* 0.567" 0.535" 0.480"

Grinding PIX S.A. (1) PI1 X C.H. (2) C.H. X S.A. (3)

"

ave. rank: 2.67 ave. I: 0.661 3 4 5 6 7

ave. r: 0.538 ave. rank: 5.50

o . 4 ~

a

0.578" 0.535" 0.480"

:I 7

ave. I: 0.531 ave. rank: 5.67

Tooth measures relating to no common~function (2.0.X S.A. (10) 0.353 ave. r: 0.322 C.O. x PI1 (9) 0.291 1: ave. rank: 9.50

1

Listed in parenthesis after each pair is the correlation rank in the unstandardized data set. Asterisk indicates the measurements are significantly greater than zero at the 99% confidence level.

length of the cristid obliqua and the length of the hypoconid traverse in Phase I of the power stroke are both measures of shearing functions; the former is a prominent shearing crest and the latter is that portion of the power stroke where shearing occurs. In all, ten pairs of measurements and their correlations were investigated. Eight of the ten pairs share at least one functional factor (table 3). Two do not: the cristid obliqua is related to neither the surface area of crushing and grinding nor the PHASE I I

PHASE I

SHEARING

CRlSTlD OBLIQUA

CRUSHING

GRINDING

CROWN HEIGHT SURFACE AREA

Fig. 2 Five of the tooth dimensions used in this study relate directly to inferred tooth functions, shearing, crushing, and grinding. Only tooth dimensions which measure the same functional factor are significantly correlated (table 3). Thus the total size of grinding surfaces is significantly correlated with the length of the second phase of mastication during which upper and lower surfaces are ground across each other.

length of the hypoconid traverse in Phase 11. Table 3 illustrates that correlation is strongly affected by tooth function: statistically significant correlations exist only between factors related to a common function. Two pairs of correlations which do not have a common functional element rank numbers 9 and 10 in overall correlation (average r equals 0.322, not significantly correlated at the 0.99 confidence level). The average correlation between tooth measurements related to shearing function is 0.661, those for crushing and grinding are 0.538 and 0.531 respectively. The differences between these average correlations are not significant. All average correlations for shearing, crushing, and grinding are significantly larger than the correlations between tooth measurements relating to no common function. All pairs of tooth measurements compared in this study are positively correlated with one another, even when the effects of body size are eliminated, implying that primates which have more highly developed shearing functions also have more crushing and grinding. In fact, more than

202

RICHARD F. KAY

average expression of one function generally indicates a greater development of each of the other two functions.

B. Molar tooth function and the energy requirements of primates Allometry describes the phenomenon of relative changes in shape during growth or relative differences in the magnitude of dimensions in species of different sizes. The relationship between a pair of morphological or physiological measurements X and Y is generally described by the equation: Logex = B

+ Y (LogeC)

where B is a constant and C is the value of the exponent of the power function relating variables X and Y. The equation states that X is proportional to Yc. When B equals zero and C equals 1.0, the ratio of X to Y is a constant regardless of size: shape is preserved (isometry). When C is less than 1.0 but greater than zero, the ratio of X to Y increases with increased body size (negative allometry). When B equals zero and C is greater than 1.0, the ratio of X to Y is decreasing with increased size (positive allometry). For mammals, the total daily energy production in kilocalories is proportional to the 0.75 power of body weight in kilograms (Kleiber, ’61). The amount of food which an animal must acquire, break down and absorb must also be proportional to the 0.75 power of its body weight, when that food is of constant accessible energy content. This relationship can be expressed in the equation E a = B -t 0.75(M) where E ais loge total energy production (kilocaloriedday), M is loge body weight in kilograms, and B is a constant. In most cases, body surfaces increase proportional to the 0.66 power of body weight. This is a special case of isometry; the square root of body surface and the cube root of body weight are proportional to each other by the exponent 1.0. Many examples of isometric surface area to body weight relationships occur in biological systems: for instance, the total surfaces of mammalian skin are proportional to the 0.66 power of body weight. In some cases, total surface areas are scaled according to an animals’ requirements for oxygen and nutrients in its metabolic processes. For example, in mammals the total surface area of the

lungs is proportional to the 0.75 power of their body weight: in mammals lung surface is isometric with oxygen consumption required for metabolism (Schmidt-Nielsen, ’72). Analysis of the data collected in this study shows that the power functions of two direct measures of shearing are negatively allometric: the length of the cristid obliqua, a prominent shearing crest, equals 0.53 +- 0.14 (95% confidence level) times the cube root of body weight (in grams) minus 0.994; the length of the second molar hypoconid path in Phase I, a measure of the importance of this phase in the power stroke equals 0.70 -+ 0.13 power of the cube root of body weight (in grams) minus 1.459. The surfaces of contact at the termination of Phase I of the power stroke are isometric with BM, the cube root of body mass (SA = BM 1.96 f 0.17 - 3.212). Put another way, the square root of surface is proportional to the 0.98 power of the cube root of body mass. The length of the second molar hypoconid traverse in Phase 11, a measure of the importance of grinding function, is also isometrically proportional to the cube root of body weight PII = BM 0.92 20.14 - 1.733). 0.92 is not significantly different from 1.0. The height of the second molar hypoconid, a measure of overall wear resistance, is isometric with BM the cube root of body weight (CH = BM 0.83 -c 0.17 - 1.207). In summary, large primates have proportionately shorter shearing blades than small primates (and tupaiids), but designs for crushing, grinding and wear resistance are proportionately the same at any size. The total energy which must be ingested by mammals in order to balance their metabolic heat production should increase proportional to the 2.25 power of the cube root of their body weight. (If E a = B 0.75(BM), and we substitute 3L for BM, where L is the cube root of M, we get Ea = B 0.75(3L), and E a = B 2.25L). The data listed above do not support the hypothesis that the “amount of food preparation” increases proportionately with the 2.25 power of the cube root of body mass. Shearing, crushing and grinding dimensions do not increase in size proportional to total energy budgets (fig. 3). The negative allometry between second molar tooth function and energy requirements

+

+

+

PRIMATE MOLAR ADAPTATIONS

could be an artifact of the choice of this tooth to assess the amount of these functions in the whole dentition. To test this possibility, the sum of the surface areas of the whole lower postcanine battery was calculated by summing the products of the lengths and breadths of their individual teeth, an estimate of the total morphological commitment to food preparation. For ten taxa ranging in size from Microcebus murinus (60 grams) to Gorilla gorilla, males, (160,000 grams). Loge x = 0.59 t 0.08 Y - 4.65

where X is the total area of mastication in square centimeters, and Y is the body mass in grams. The range for the slope represents the 99% confidence interval and indicates that this power function is not significantly different from 0.66, but is significantly smaller than 0.75, the exponent expected if surface area were isometric with energy intake requirements to balance metabolic heat production. Thus, no matter how it is measured, the expres-

2 0

LOG,

LO

CUBE R O O T BODY M A S S

Fig. 3 The Loge of the cristid obliqua (in mm.) equals 0.535 times the logecube root of body mass (in gr.) minus 0.994. The 95% confidence interval for the estimate of the slope is 0.139. The dashed line on the graph is the predicted changes in the length of a shearing blade if it followed the curve for metabolic rate. [Ea is proportional to 2.25(L) where Eais the total energy production (Kcallday), and L is loge cube root body mass: see text for derivation]. Symbols: I, Specialized insectivores; F, specialized frugivores; L, specialized folivores. Primate frugivores tend toward, but do not always have, shorter shearing blades than do folivores or insectivores of the same body although this is the most common pattern.

203

sion of individual tooth functions and the total morphological commitment to food preparation is not simply related to changes in food requirements with body mass. The implications of this finding are unclear, but luckily large primates do not starve to death because of it. For more discussion see Kay (’75). C . Food preparation and dietary

specializations Primate diets consist of varying proportions of three principal foods: plant material high in structural carbohydrate fractions (usually leaves, bark and pith), plant materials high in nonstructural carbohydrate fractions (fruit and sap), and animal foods. These foods presumably require different amounts of food preparation and perhaps different proportions of shearing, crushing and grinding. To clarify this relationship, dental comparisons were made between primates with differing food preferences. Each species used was identified as a specializer in one of the above categories if i t consumed 45% or more by weight of its food in that category. Although foods which make up less than 45% of an animal’s diet may be nutritionally important, it is assumed that large amounts of food must be habitually ingested before its physical properties have a selective influence on molar design. In the future such a classification may have to be refined to express the special selective influence of particular food items. Although each dietary category includes many kinds of foods, these categories are referred to for convenience in this study as leaves, fruit, and insects, according to the principal kinds of materials contained in each. The diets of the primate species used in this study are presented in table 4. Leaf, fruit, and insect eaters were segregated and regressions were calculated between loge of body mass and loge of each tooth measurement (table 5 ) . Two measurements of shearing function were examined: (1) The exponent of the power function relating the cristid obliqua length and body size is the same in fruit and leaf eaters, but it is significantly larger among insect eaters. The Y intercept for insectivores is significantly smaller than that for leaf or fruit eaters. Thus insectivores and leaf eaters have significantly longer shear-

Microcebus murinus (F)

Phaner furcifer (F)

Tupaia glis (I) Cheirogaleus major (F)

Species

Leaves, flowers, bark, some fruit Leaves, buds, bark, some fkuit Leaves, flowers, some fruit Fruits and insect larvae; proportions not known Chiefly insects and some small vertebrates Fruits, leaves, shoots, eggs and young birds 85% animal prey, especially noxious insects; 14% fruits Principally fruit and gum; some insects

75% fruit; 25% animal prey; possibly more insects Largely insects, also fruit, gum flowers and buds

Propithecus verreauxi (L)

Avahi laniger (L) Indri indri (L) Daubentonia madagascariensis (?F)

Nycticebus coucang (F)

Arctocebus calabarensis (I)

Galago alleni (F)

Galago demidovii (I)

Perodicticus potto (F)

Loris tardigrudus (I)

Lemur rubriventer (?L) Lemur variegatus (?L) Hapalemur griseus (L)

Lepilemur mustelinus (L)

Mostly insects, some fruit Predominantly fruits, flowers, honey, some insects Resins, insect secretions, nectar; possibly more insectivorous than Cheirogaleus Primarily fruit but will eat insects

Diet

Leaves, bark, flowers; some fruit Fruit, wild figs, bananas; also leaves, herbs, flowers. In some areas spends more time eating leaves Leaves SO%, fruit 50% Leaves 5 0 % , fruit 50% Leaves, flowers bark and fruit; especially fond of reeds Leaves, flowers, bark and some green fruit

Lemur fulvus (L) Lemur catta (F)

4

Petter, '62a Petter, '62a Hladik and Charles-Dominique, '74; Petter, '62b; Webb, '54; Petter and Peyrieras, '70 Charles-Dominique and Hladik, '71 ; Forbes, 1894; Hladik et al., '71; Petter, '62a,b Hill, '57; Grzimek, '68; Forbes, 1894; Petter, 62a,b; Rand, '35; but see Jolly, '67 Grzimek, '68; Hill, '57; Petter, '62a,b Attenborough, '61; Grzimek, '68; Petter, '62a,b Forbes, 1894; Elliot, '13; Grzimek, '68; Petter, '62a,b Amerasinghe et al., '71; Forbes, 1894; Hill, '57; Hladik and Hladik, '72; Petter and Hladik, '70; Phillips, '35; Subramonian, '57 Banks, '49; Elliot and Elliot, '67; Harrison, '49; Harrison, '62; Wroughton, '16 Charles-Dominique, '71 a; Durrell, '49; Jewell and Oates, '69 Allen and Lawrence, '36; Bearder and Doyle, '74; Charles-Dominique, '71a, '74; Hollister, '24; Jewell and Oates, '69; Jones, '69; Loveridge, '56; Oates, '66;Malbrant and Maclatchy, '49; Turner, '14; Van Bosman quoted in Rosevear, '35 Charles-Dominique, '71a, '74; but see Jewell and Oates, '69; Oates, '66 Charles-Dominique, '71a,b, '74; Jewell and Oates, '69; Malbrant and Maclatchy, '49

Forbes, 1894; Martin, '71; Shaw, 1871; but see Petter, '62a,b, '65; Webb, '54 Sussman, '74; Rand, '35 Jolly, '67; Petter, '62a; Rand, '35; Shaw, 1879; Sussman, '74

Hill, '57; Petter, '62a, '65; Petter et al., '71

Medway, '66 Petter, '62a; Shaw, 1879

References

The diet of the species used in this study. The letter i n parenthesis at the right of the species indicates a dietary specialization ( F , Fruit; I, Insects; L , Leaves)

TABLE

Chiefly insects and small lizards Fruits, berries, nuts, insects, tree frogs, small birds Fruits and nuts, 60% ; leaves, buds, flowers, gum, 10% ; animal prey 30% Fruits and nuts, 65% ; leaves, bark, flowers, gum, 30% ; animals, 5% Almost entirely fruit Almost entirely fruit Mixed fruit and leaves; leaves, flowers, buds, 59% ; fruit, 41% Fruit and insects; 65% fruit and nuts; animals, 20% ; leaves, buds, bark, pith, flowers, gum, 5% Mainly fruit, some insects Fruit and nuts, 90% ; some insects and leaves Berries, figs, bananas Spends more than twice as much time eating leaves, flowers, and buds a s it does feeding on fruit Specialized in both leaves 50% and fruit 50%

Considerable amounts of fruit Strong specialization i n fruit; also some leaves, small amounts of animal food

Mostly herbivorous (non-frugivorous);pith, bark, leaves

Tarsius spectrum (I)

Cullithrix jacchus (? F)

Pithecia pitheciu (F) Chiropotes satanas (F) Alouatta villosa (L)

Cebus capucinus (F)

Ateles geofloyi (F)

Hylobates klossi (F)

Symphalangus syndactylus (L)

Pan paniscus (F) Pan troglodytes (F)

Gorilla gorilla gorilla

Pongo pygmaeus (L)

Saimiri sciureus (F)

Aotus trivirgatus (F)

Suguinus geoflroyi (F)

Galago elegantulus (F)

Fruit, berries and gum; also insects, birds and their eggs; buds Mainly gum; also some fruit and insects

Galago crassicaudutus (F)

Booth, '60;Malbrant and Maclatchy, '49; Jones and Sabater-Pi, '71;Forbes, 1894; Schaller, '63,'65a

'66,'69

Azuma and Toyoshiama, '61-'62; Forbes, 1894; Gartlan and Strusaker, '72;Goodall, '63,'65; Haddow et al., '47;Itani and Suzuki, '67; Irsac, '67;Jones and Sabater-Pi, '71;Kano, '71b;Malbrant and Maclatchy, '49;Nissen, '33;Reynolds, '65;Reynolds and Reynolds, '65;Schaller, '65b;Sugiyama, '68;Suzuki,

Especially Carpenter, '38;Davenport, '67; Mackinnon, '71;but see Banks, '49;Harrison, '60;Schaller, '61;Wallace, 1869; A. Horn (personal communication)

Allen, '16;Fooden, '64;Forbes, 1894;Humboldt and Bonpland, 1811 Bates, 1863;Carpenter, '35;Hladik et al., '71; Sanderson, '49;Thorington, '67,'68 Tenaza and Hamilton, '71;(for other species see especially Carpenter, '40;Chivers, '72) Chivers, '72

Enders, '30;Hladik, '70;Hladik and Hladik, 69;Hladik et al., '71;Moynihan, '70 Gumilla, 1759,quoted i n Humboldt and Bonpland, 1811;Hladik and Hladik, '69; Moynihan, '64 Fooden, '64;Sanderson, '49 Fooden, '64;Forbes, 1894 Altmann, '59;Carpenter, '34,'65;Hladik, '70, '72;Hladik and Hladik, '69;Hladik et al., '71; Richard, '70 Enders, '35,Hladik, '70;Hladik and Hladik, '69;Hladik et al., '71

Ansell, '60;Allen and Loveridge, '40;Bearder, and Doyle, '74;Forbes, 1894;Smithers, '66 Charles-Dominique, '71a,'74;Jewell and Oates, '69;Smithers, '66 Forbes, 1894;see Davis, '62;Fogden, '74 for other species Grzimek, '58

RICHARD F. KAY

206

TABLE 5

Exponents ( B ) u n d intercept values (A) f o r t h e equutions relating t h e loge of e a c h tooth m e a s u r e m e n t a n d the loge of t h e c u b e root of body m a s s together with their 95% confidence intervals f o r t h e p r i m a t e s of three specialized dietary groups Tooth Length

Cristid obliqua

-

A

B

A

B

Insectivores

- 1.55t0.21"

1.54%1.44

-2.97-tO.15"

1.88k 1.01"

Frugivores

--0.71 % 0.05"

0.84 % 0.09

- 0.99 2 0.09"

0.45 -C 0.18

Folivores

-- 0.40 +- 0.04"

0.82 2 0.07

-0.57t0.08"

0.47&0.15

Insectivores

- 1.15%0.08"

Crown Height

J

Frugivores

- 1.40% 0.09

7

Phase I

0.94 k O . 5 7

- 1.78t0.38

1.0722.57

0.85% 0.18

- 1.55 t 0.08

0.67 t 0.14

0.83%0.09

-1.44k0.12

0.7520.21

I

Folivores

- 1.10%0.05*

Phase I1 Insectivores Frugivores Folivores

- 1.352 0.28" J - 1.93k0.07 \

- 1.38% 0.09^

Crushing surface

0.762 1.88

- 1.84%0.45*

0.96k0.12

- 3.57& 0.14

0.84+0.16

- 3.62 % 0.14

1

1.4023.11 2.03 % 0.26 2.13 +- 0.26

Asterisks which follow any entry indicate that the entry is significantly different at the 95% confidence interval &om an entry for a.nother dietary category and an arrow indicates the particular dietary group from which it significantly differs. If all dietary categories are distinct, no arrows are included.

ing blades than do fruit eaters of the same different at the 99% confidence interval body weights. In insectivores the differ- for any pair of dietary groups. The Y inence results from a larger exponent while tercept value for insectivores and leaf in leaf eaters the difference is in the Y eaters is not significantly different but intercept while the slope is similar. Fig- both have significantly larger intercept ure 3 illustrates this point. ( 2 ) The expo- values than frugivores. One measure of overall wear resistance nent of the power function relating the length of the Phase I hypoconid traverse was made, the crown height at the second and body size is the same for all dietary molar hypoconid. The exponents of the power function relating this measurement groups. Three direct measures of crushing and to body mass are not significantly different grinding functions were used. (1) The ex- for any pair of dietary groups, but the Y ponent and intercept of the regression of intercept values are significantly larger the length of the Phase I hypoconid tra- for insectivores and leaf eaters than for verse and body weight has already been frugivores. The combined evidence indicates that described. (2) The exponent of the power function relating second molar crushing primate frugivores have less well developed and grinding surfaces to body mass is not molar features for wear resistance and all significantly different at the 99% confi- modes of food preparation than do either dence level for any dietary group, but the primate insectivores (and Tupaia) or priY intercept is significantly smaller for in- mate leaf eaters. The second molars of sectivores than it is for frugivores or leaf frugivores tend to have similar shapes to eaters. The Y intercepts for the latter two folivores and insectivores, but at smaller do not significantly differ. (3) The expo- body sizes: the exponents of the power nent of the power function relating the function relating each tooth measure and length of the Phase I1 second molar hypo- body mass are usually not signlficantly conid traverse, during which grinding oc- different between any pair of groups but curs, to body mass is not Significantly the Y intercepts for frugivores are smaller.

207

PRIMATE MOLAR ADAPTATIONS

None of the allometrically adjusted tooth dimensions have the power to discriminate folivorous from insectivorous species, but this is possible based on body size in conjunction with tooth dimensions. Insectivorous primates and tree shrews are invariably smaller than primates which feed on leaves. The largest primate insectivores are Loris tardzgradus and Arctocebus calabarensis. Each species has an adult body mass of about 200 grams, whereas the smallest folivorous primates are Avahi luniger and Lepilemur mustelinus which have masses of around 1000 grams and 800 grams respectively. This order of magnitude difference in body size probably relates to the availability and nutritional content of these foods. Insects are high in energy but unavailable in sufficient quantities to sustain a large animal. Exceptional mammalian insectivores which attain large size specialize in social insects (ants, termites) which are abundant but often require special tools to reach (digging claws, long tongues). In contrast leaves are abundant but low in nutrition: small mammals with high metabolic rates can not process enough bulk to balance their energy budgets.

D. Principal coordinates analysis of tooth shape and diet It has been shown above that insectivorous and folivorous groups are distinct from frugivores in having relatively large teeth with well developed shearing, crushing and grinding features, and that while the first two groups have similar molar structure, leaf-eaters are always larger than insectiviores. However, table 6 illustrates that individual dimensions do not always assign a species to its known dietary group. For example, while 19 frugivorous species have shorter than average cristid obliquas, three do not. A principal coordinates analysis was undertaken to see whether this multivariate method would provide a more complete morphological separation. The measurements were standardized using the “% - difference” technique so that each tooth dimension could be compared to that of all the other species regardless of body size differences. The first principal coordinate in the analysis, accounted for 38% of the total variability within the data (tables 7, 8).

TABLE 6

Dietary specialization u n d tooth structure

Tooth measure

Cristid obliqua (shearing) Frugivores Folivores Insectivores Crown height (wear resistance) Frugivores Folivores Insectivores Phase I traverse (shearing, crushing) Frugivores Folivores Insectivores Phase I1 traverse (grinding) Frugivores Folivores Insectivores Surface area of crushing (crushing, grinding) Frugivores Folivores Insectivores Tooth size (length of M2) (total tooth design) Frugivores Folivores Insectivores

Species with Species with more than less than average ex- average expression of pression of the feature the feature

3 14 4

19 1 1

3 12 5

19 3 0

2 10 4

20 5 1

4 11 4

18 4 1

3 7 5

19 8 0

1 13 4

21 2 1

A regression was fit for each tooth dimension with body mass. Each taxon was scored according to whether it falls above or below the regression line. A comparison between feeding groups illustrates the general tendency for insectivores and folivores to have bigger dimensions (for their body size) than the empirical average for primates and Tupaia: the reverse i s true for frugivores.

A plot of the first and second principal coordinates is presented in figure 4. Primate frugivores (octagons) all fall to the left of the value 0.2 on the first coordinate (except for Galago alleni: see Note added in proof). Those species which scored greater than 0.2 on the first principal coordinate are specialized leaf eaters (triangles) or insect eaters (squares). The molar teeth of Daubentoniu madagascariensis resemble those of frugivores. Little is known of the aye-aye in the wild state but Petter and Petter (’67) reported that Daubentonia specializes in grubs and other soft bodies insects, although they confirmed that this species will readily take a variety of fruits in captivity. On the basis of its molar tooth morphology,

208

RICHARD F. KAY TABLE 7

TABLE 8

First f o u r eigenualues of t h e transformed ussociat i o n m a t r i x of a principal coordinates analysis of the percentage differences b e t w e e n observed a n d expected tooth m e a s u r e m e n t s . See t e x t for f u r t h e r discussion

Scores of t h e frrst four principal coordinates extracted f r o m a n analysis of the percentage difference b e t w e e n expected and observed t o o t h m e a sures

Eigenvalues

1. 3.7890663

2. 1,1197309 3. 0.8258893 4. 0.5715379

~~

Taxon

I

96 “variance”

37.5 10.9 7.9 5.5

Trace of the diagonal elements of the transformed association matrix = 10.39262.

Daubentonia is apparently a specialized frugivore (as here defined) which takes additional quantities of soft bodied insects requiring little preparation. The same conclusion could be reached on the basis of body size: no living primate insectivore has attained the body size of Daubentnonia. An extinct species of this genus attained even larger size. Alternatively, a rough parallel could be made between Daubentonia and other arboreal mammals such as myrmecophagids and manids which feed on social insects (i.e., termites, ants, and the like). Species of both families have undergone extreme dental reduction (more so than in Daubentonia) and have attained an unusually large body size for insectivores. The results for lorises are in accord with dietary information except in the case of Galago alleni. See Note added in proof. Until recently, limited data from field studies gave indications that the food of Pongo pygmaeus was predominantly fruit. MacKinnon (’72) has shown that the yearly diet includes about 50% fruits and 50% folivorous materials. Not surprisingly therefore, Pongo plots among the folivores on the basis of the morphology of its molar teeth. Another primate assumed until recently to be frugivorous is Symphalangus syndactylus. However, its assignment to the folivores by molar morphology is supported by a recent field study of Chivers (’72). Pan species plot as frugivores while Gorilla plots as a folivore. Data are limited on the diets of lemurines. The best known species are Lemur catta, Lemur fulvus, Lepilemur mustelinus and Hapalemur griseus (for citations see table 4). Of these, Lemur catta is largely frugivorous and Lemur fulvus, Hapalemur

I1 F2 L10 L9 L12 L7 L14 F6 F12 F11 L8 L15 L11 F15 I4 I2 F14 F7

F1 F8 I5 I3 F19 F20 F13 F5 F16 L1 L2 F18 F17 F2l F22 F10 L13 L4 L3 F9 F3 F4 L5 L6

0.609 - 0.025 0.218 0.200 0.143 0.368 0.071 - 0.226 - 0.262 - 0.258 0.253 0.067 0.186 - 0.359 0.160 0.567 - 0.342 - 0.135 0.263 - 0.122 0.220 0.352 - 0.330 - 0.414 - 0.295 -0.115 -0.417 0.422 0.514 - 0.445 - 0.427 - 0.414 - 0.431 - 0.247 0.109 0.296 0.437 - 0.201 - 0.042 - 0.127 0.167 0.010

I1

- 0.093 -0.159 - 0.214 - 0.131 0.065 0.051 0.044 - 0.215 0,199 0.208 0.038 0.491 - 0.063 - 0.037 - 0.056 - 0.220 - 0.074 - 0.362 0.058 0.257 0.257 -0.142 - 0.080 0.005 - 0.076 - 0.059 - 0.251 0.119 -0.111 - 0.017 - 0.075 0.033 0.253 - 0.162 0.049 0.123 0.144 0.023 - 0.002 0.067 0.100 - 0.080

I11

0.092 - 0.091 - 0.074 - 0.049 0.071 0.111 0.128 - 0.014 - 0.023 - 0.039 - 0.046 0.017 0.142 - 0.144 0.018 0.134 - 0.047 0.031 - 0.136 - 0.102 0.171 0.042 0.042 - 0.053 -0.180 - 0.038 0.085 0.227 0.57 0.056 -0.118 0.096 - 0.049 - 0.312 0.042 - 0.240 0.056 0.109 0.087 0.113 0.051 - 0.148

-

IV

0.023

- 0.235 - 0.056

0.131 0.077 0.041 -0.135 0.038 - 0.021 0.069 0.206 0.085 0.043 0.052 0.169 0.124 - 0.128 0.213 0.056 0.029 0.088 0.065 0.137 -0.100 0.094 - 0.036 0.051 0.061 0.023 0.195 - 0.039 0.190 - 0.132 0.247 - 0.096 0.037 - 0.041 - 0.002 - 0.050 - 0.035 0.193 - 0.082

All six tooth measurements were considered. For detailed discussion see text. Forty-two taxa were used, the symbols are identified in the legend to figure 4. I, Insectivores; F, Frugivores; L, Leaves.

and Lepilemur are predominantly folivororous. On the basis of tooth morphology Lemur catta falls at the border between folivores and frugivores while Lepilemur and Hapalemur would be categorized as folivores. Lemur fulvus was not considered in this study. Two other lemurines with poorly documented diets were considered: Lemur rubriventer and Lemur variegatus. These would be classified as folivores on the basis of their molar tooth structure.

PRIMATE MOLAR ADAPTATIONS

209

A15

II

0.4

0 5

016

07

Fig. 4 The first two coordinates of a principal coordinates analysis of the molar dimensions of non-cercopithecoid primates and tree shrews (all standardized for body size). On the first axis frugivores cluster to the left, folivores and insectivores to the right. None of the coordinates segregate insectivores from folivores. See text for further discussion. Insectivores (squares): 1, Tupuiu glis; 2, Arctocebus cultrbarensis; 3, Tursius spectrum; 4, Loris turdigrudus; 5 , Gnlago demidouii; Leaf-eaters (Folivores) (triangles): 1, Alouci ttu uillostc males; 2, Aloztattu uillosa females; 3, Pongo pygmueus females; 4, Pongo p y g m u e u s , males; 5 , Gorillu gorilltr males; 6, Gorilltr gorillu females; 7, Hapulemzcr griseus; 8 , Propithecus uerreauri; 9, L e m u r f u l u u s ; 10, Lemur ntbriuenter; 11, Indri indri; 12, Lemur uuriegutus; 13, SymphuIn ngzc s s yndirc ty lus; 14, Lep ilemur m u s telinu s; 15, Avtchi la nig er, Fru givores (octagons): 1, Gulugo trlleni; 2, L e m u r cuttii; 3, Pun troglodytes males; 4, Pun troglodytes females; 5 , Pitheciu pitheciu; 6, Cheirogtrleus mtdor; 7, Gnlago crussictcccdutus; 8, Gulugo eleguntulus; 9,Pun puniscccs; 10,Hylobates klossi; 11, Phicnerfurcifer; 12,Microcebirs murinus; 13,Aotus triuirgtrtus; 14, Perodicticus potto; 15, Duubentoniu mcidcrgccscuriensis; 16, Chiropotes scctunus; 17, Cebzts cupucinus females; 18, Cebus cctpucinccs males; 19, Catlithrix jacchcis; 20, Snngzcinzts geoffroyi; 21,Suimiri sciicrezts; 22, Ateles geoffroyi.

The morphological analysis for New World monkeys accords well with the detailed behavioral information of Hladik and Hladik (‘69) that Aotus, Cebus, and Saguinus are primarily frugivorous, and Alouatta is much more folivorous. Callithrix and Saimiri for which little dietary information is available would be classified as frugivores. There is undoubtedly great variation in the amounts of insects eaten by “frugivorous” species. That first and subsequent principal components do not discriminate between foli-

vores and insectivores confirms the hypothesis that both diets select for molar tooth structure in similar ways. Both groups tend to have better expression of characters relating to shearing, crushing and grinding functions than average primates to their size, Since members of these dietary groups do not overlap in body size, the addition of this criterion would effect their complete separation. The second principal coordinate accounts for 10.9% of the total variability of the system, while the third accounts for

210

RICHARD F. KAY TABLE 9

Eigenvalues, percentages of variunce und factor scores for principal components analysis of tooth meusurements stundurdized for body size Eigenvalue

Percentage of variance

3.94 0.87 0.56 0.32 0.20 0.10

65.7 14.5 9.3 5.4 3.3 1.7 Factor scores

Variable

Length Mz Cristid obliqua Crown height P I traverse PII traverse Surface area

Factor 6

Factor 1

Factor 2

Factor 3

Factor 4

Factor 5

- 0.92451

0.06821 0.53917 0.10400 0,17624 -0.57462 - 0.44773

0.15155 -0,01748 0.37514 - 0.38384 0.27583 - 0.41592

0.03097 0.10695 - 0.34171 0.17880 - 0.30357 - 0.26510

0.29051 0.08929 - 0.20000 - 0.23477 - 0.06444 0.09563

- 0.80358

- 0.83162 - 0.84825 -0.70136 - 0.73547

7.9%. Subsequent axes fall off in the percentage of attributable variability.

E. Principal components analysis of primate molar teeth A principal components analysis was run on the “percentage-difference” data described above. The first principal component accounts for 65.7% of the variance in the system, the second for 14.5% and the third for 9.3%; in all a total of 89.5% of the variance is represented by these axes. The factor loadings for each principal component are listed in table 9 . Principal component I has a roughly equal loading for each of the original variables measured. Animals with consistently large variables will be separated from those which have small variables. Since data used here have been transformed to eliminate the effects of absolute size, animals which have consistently larger tooth dimensions than would be expected for their size are being separated from those which have consistently smaller dimensions. Since frugivores tend to have less expression of the molar features associated with food preparation, they separate readily from insectivores and folivores which prepare their food more as judged by the greater than average development of design features associated with shearing, crushing and grinding functions on their molars. The first principal component, therefore, in interpreted as a “food preparations” axis.

-

0.17973

- 0.20939 0.01005 0.12245

- 0.07428 - 0.07891

Principal component I1 is dominated by the positive influence of the cristid obliqua length on the one hand and the negative influence of the length of Phase I1 traverse

”i

0

2

LOG.

3

C U e E ROOT S O D Y M A S S I N G R A M S

Fig. 5 Because the allometric coefficients of different dental dimensions differ, tooth shape changes irrespective of diet. Here the linear dimension of the areas of crushing and grinding and the length of a shearing blade (cristid obliqua) are plotted against body size. A s a n example, Alouatta and Lepilemur, both folivores, differ from comparable sized frugivores in having better developed shearing and grinding features. But Alouattu also differs from Lepilemur in body size; the former weights about 7,000 grams, the latter about 800 grams. Because of this Alouatta differs from Lepil e m u r in having a larger ratio of the square root of crushing surfaces to shearing blade length; for Alouutta the ratio is 1.53, for Lepilemur it is 0.88. The larger the size disparity the less informative will be this ratio. Comparing a 100,000 gram primate with a 100 gram one would give 3.01:0.98.

PRIMATE MOLAR ADAPTATIONS 100 GRAM

PRIMATE

. IMM

INSECT IVOR E

FRUGIVORE

TOOTH SHAPE AND DIE7

Fig. 6 Idealized scale drawings of the second lower molars of a hypothetical primate frugivore and insectivore both weighing 100 grams based on empirical regressions between tooth dimensions and body mass for these groups. This illustrates that there is a large size disparity between the teeth of species with different diets when they have the same body size. Scale bar is 1 mm.

and the surface area of crushing on the other. In the third principal component, animals with comparatively high crowns and large amounts of Phase I1 shearing, together with comparatively small amounts of Phase I1 movement and small crushing surfaces are separated from animals with low crowns, small amounts of Phase 11, large crushing surfaces and well developed Phase I. Neither principal component aids in the dietary discrimination nor does it appear to identify any apparent functionally significant differences. CONCLUSIONS

Numerous authors have indicated that there is a strong general relationship between molar tooth structure and diet (e.g., Osborn, 1895; Gregory, '22) and between molar tooth function and jaw movement (e.g. Hunter, 1771, 1861, Ryder, 1878, 1879; Gregory, '20; Butler, '52, '73; Butler and Mills, '73; Gingerich, '74; Mills, '55). However, the specific relationship between food preparation and dietary specializations have never been considered together in a systematic manner. The inferred relationship between those two factors can now be clearly outlined for non-cercopithecid primates and Tupaia. Three principal facts have emerged: (1) When the effects of body size are eliminated, correlations are higher between

21 1

second molar measurements related to a common function design (shearing, crushing, grinding) than between functionally unrelated measurements. Average correlations between measurements which relate to shearing, crushing and grinding appear to be the same. (2) Although daily energy requirements in kilocalories in mammals increase by the 2.25 power of the cube root of body mass and the surfaces across which foods are absorbed may increase proportional to these requirements, (Kay, '73), neither the linear dimensions nor surfaces of teeth increase at this rate: second molar shearing, crushing and grinding tooth designs increase at significantly lower powers of the cube root of body mass than do energy requirements. A measure of the overall size of the postcanine dentition also indicates that its size is negatively allometric with metabolic energy needs. ( 3 ) The total amount of food preparation as inferred from measures of shearing, crushing and grinding design on molars is consistently greater among primates which specialize in diets of leaves or insects than it is among primate frugivores of the same body size. It has been shown that living primates that specialize in leaf eating do not overlap in absolute body size with those that specialize in insect eating (Kay, '73). Thus, it is possible from the combined data of body weight and dental dimensions to completely segregate specialized frugivores, insectivores and leaf eaters. The results of the present study show that the various functional systems in primate molars have different allometric coefficients. At different body sizes, primates will have differently shaped molars irrespective of their dietary specializations. To take an example, the linear dimensions of the surface areas of crushing and grinding on second lower molars change at a greater rate with respect to body mass than does the length of the second lower molar. In contrast, the length of a shearing blade on the second lower molar changes at a lower rate with respect to body mass than does tooth length. This means that an average primate weighing 100,000 grams will have a second lower molar with disproportionately expanded crushinglgrinding surfaces and reduced shearing blades when compared to a primate weighing 100 grams (fig. 5). However, at the same body

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size a primate which is adapted to eat leaves will have proportionately larger crushing and grinding surfaces and longer shearing blades than will a primate frugivore. Similarly an insectivore will have larger crushinglgrinding surfaces and longer shearing blades than a frugivore at the same size (fig. 6). It is emphasized that an effective assessment of the behavioral modifications implied by morphological trends in primate molar evolution depends on the isolation of allometric factors. ACKNOWLEDGMENTS

I thank Drs. E. L. Simons, D. R. Pilbeam, J. H. Ostrom, A. W. Crompton and K. M. Hiiemae for their valuable comments on this manuscript. Drs. W. Hylander and M. Cartmill aided in its conversion into English. LITERATURE CITED Allen, G. M., and B. Lawrence 1936 Scientific results of an expedition to rainforest regions in eastern Africa, Part 111, Mammals. Bulls. Mus. Comp. Zool., Harvard, 79(31. Allen, G. M., and A. Loveridge 1942 Scientific results of a fourth expedition to forested areas in east and central Africa, Part I, Mammals. Bull. Mus. Comp. Zool., Harvard, 89: 145-214. Allen, J. A. 1916 Mammals collected on the Roosevelt Brazilian expedition, with field notes by Leo E. Miller. Bull. Am. Mus. Nat. Hist., 35:

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~

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Note added in proof: Galago alleni is predominantly frugivorous (table 4) but in the dental analysis plots with insectivorous species (fig. 4). This result is inaccurate. The dental dimensions for G . alleni were based on two American Museum specimens which were allometrically adjusted using body weights from Charles-Dominique ('71a). Restudy of these specimens shows that they are larger than those of Charles-Dominique. A new regression adjustment using a more accurate body weight estimate indicates that G. alleni has smaller teeth than average for a primate of its body size. This is a pattern found among frugivorous species and not seen among primate insectivores.

The functional adaptations of primate molar teeth.

The Functional Adaptations of Primate Molar Teeth RICHARD F. KAY Department of A n a t o m y , Duke University Medical Center, D u r h a m , North Car...
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