Teeth, Brains, and Primate Life HistoriesLaurie R. Godfrey,1* K.E. Samonds,2 W.L. Jungers,2 and M.R. Sutherland3

1Department of Anthropology, University of Massachusetts at Amherst, Amherst, Massachusetts 01003-48052Department of Anatomical Sciences, School of Medicine, State University of New York at Stony Brook,Stony Brook, New York 11794-80813Statistical Consulting Center, Graduate Research Center, University of Massachusetts at Amherst,Amherst, Massachusetts 01003-4535

KEY WORDS dental development; diet; cranial capacity; life histories; primates

ABSTRACT This paper explores the correlates of vari-ation in dental development across the order Primates.We are particularly interested in how 1) dental precocity(percentage of total postcanine primary and secondaryteeth that have erupted at selected absolute ages and lifecycle stages) and 2) dental endowment at weaning (per-centage of adult postcanine occlusal area that is present atweaning) are related to variation in body or brain size anddiet in primates. We ask whether folivores have moreaccelerated dental schedules than do like-sized frugivores,and if so, to what extent this is part and parcel of a generalpattern of acceleration of life histories in more folivorous

taxa. What is the adaptive significance of variation indental eruption schedules across the order Primates? Weshow that folivorous primate species tend to exhibit morerapid dental development (on an absolute scale) than com-parably sized frugivores, and their dental developmenttends to be more advanced at weaning. Our data affirm animportant role for brain (rather than body) size as a pre-dictor of both absolute and relative dental development.Tests of alternative dietary hypotheses offer the strongestsupport for the foraging independence and food processinghypotheses. Am J Phys Anthropol 114:192–214, 2001.© 2001 Wiley-Liss, Inc.

Life history theory has grown enormously over thepast several decades. Its focus has shifted away frombody size as an “explanation” for the “fast-slow” con-tinuum described by early theorists (Taylor, 1965;MacArthur and Wilson, 1967; Peters, 1983; Calder,1984). Modern life history theory attempts to ex-plain why strong correlations hold, across so manytaxa, between body size, longevity, and so on. Envi-ronmental stability, adult mortality, and body sizeoptimization have figured prominently in life historytheory as it has developed over the past severaldecades (MacArthur and Wilson, 1967; Pianka,1970; Promislow and Harvey, 1990; Charnov, 1991,1993; Stearns, 1992; Kozlowski and Weiner, 1997).

With few exceptions (Smith, 1989, 1992; Smith etal., 1994), dental development is not often consid-ered in studies of life history variation. There areseveral reasons why dental development might be ofgreat interest to students of mammalian life histo-ries, however: 1) Dental development may providean important key to understanding the ontogeneticacquisition of ecological competence in the life his-tories of primate species. Weanlings belonging todifferent primate species are not equally ecologicallycompetent; the relationship between dental eruptionand weaning may elucidate that variation. 2) Therelative timing of aspects of skeletal and dental de-velopment may or may not be related in a predict-able manner to body size or reproductive parametersthat tend to describe the classic (“fast-slow”) lifehistory continuum. 3) Dental development provides

a means through which life history inferences maybe drawn for extinct species, as long as the relation-ship between dental development and life historyvariation among their extant relatives is well under-stood (Smith, 1989; Morbeck, 1997; Dirks, 1998;Reed et al., 1998; Kelley, 1999; Godfrey et al., inpress, a). This requires detailed analyses of theadaptive significance, in behavioral ontogeneticterms, of the timing of dental eruption.

This paper explores the relationship between den-tal development and other variables (such as age atweaning, age at first female breeding, body size,brain size) that are more commonly considered instudies of mammalian life history variation. Ourtask is not to test competing explanations of lifehistory variation (i.e., the models of MacArthur andWilson, 1967; Charnov, 1991, 1993; Kozlowski andWeiner, 1997). Such an endeavor would require con-sideration of birth and mortality rates for individu-als in different life cycle stages across species (e.g.,Ross and Jones, 1999). Rather, we are interested inbody size, brain size, and diet as possible correlatesof variation in primate dental development. We limit

Grant sponsor: NSF; Grant number: GER 9450175, SBR-9630350.

*Correspondence to: Laurie Godfrey, Department of Anthropology,Machmer Hall, Box 34805, University of Massachusetts, Amherst,MA 01003-4805. E-mail: lgodfrey@anthro.umass.edu

Received 12 July 1999; accepted 19 November 2000.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 114:192–214 (2001)

© 2001 WILEY-LISS, INC.

our discussion to the postcanine teeth, as the timingof canine eruption may be affected by factors relat-ing to the ontogeny of agonism, and should be con-sidered in conjunction with studies of the evolutionof sexual dimorphism.

We tested six hypotheses that might explain vari-ation in the pace of dental development in nonhu-man primates. Two link development to aspects ofadult size; four relate development to diet (food pro-cessing needs, the quality of the diet, or the spatio-temporal distribution and abundance of preferredfood resources). Most of the hypotheses put forthhere were constructed to explain variation in skele-tal “development” and not the development of thedentition per se. Only the brain pleiotropy and foodprocessing hypotheses make explicit predictions re-garding dental development. Our hypotheses are notnecessarily mutually exclusive, as some of our ex-planatory variables (folivory, relative brain size,amount of protein in the diet, and so on) are them-selves correlated. Folivorous species might experi-ence more rapid development than like-sized frugi-

vores as a corollary of more accelerated growth andskeletal maturation, earlier brain maturation, rela-tively small adult brain size, rapid acquisition ofecological independence, low intraspecific feedingcompetition, and/or the mechanical requirements forbreaking down leaves and seeds. Insectivorous pri-mates might experience rapid development as a cor-ollary of their small brains, small bodies, and/orhigh protein diets. It is only through an examinationof the complex interrelationships among possibleexplanatory variables that we can hope to under-stand dental developmental differences across theorder Primates.

MATERIALS AND METHODS

Samples

Dental eruption and metric data were collected byK.E.S. and L.R.G. on 900 individuals (465 imma-tures, and 435 adults) belonging to 40 species in 11families of nonhuman primates (Table 1). Becausethere is little published information on the dental

TABLE 1. Samples of measured crania1

Family Genus and species Dietary category Immature individuals Mature individuals

Indridae Propithecus tattersalli 3 1 1Propithecus verreauxi 3 21 25Propithecus diadema 3 13 30Avahi laniger 3 8 17

Lemuridae Varecia variegata 2 11 6Hapalemur griseus 2 11 7Lemur catta 2 16 11Eulemur macaco 2 6 8Eulemur fulvus 2 20 8

Lepilemuridae Lepilemur ruficaudatus 3 6 14Galagonidae Galago moholi 1 15 14Callitrichidae Callithrix jacchus 1 7 6

Saguinus nigricollis 1 8 9Saguinus fuscicollis 1 2 7

Cebidae Saimiri sciureus 1 4 6Cebus albifrons 2 14 10Cebus apella 2 12 10Aotus trivirgatus 2 4 9

Atelidae Alouatta palliata 3 9 10Alouatta caraya 3 5 7Ateles geoffroyi 2 16 17

Cercopithecidae Chlorocebus aethiops 2 16 8Macaca fascicularis 2 28 15Macaca mulatta 2 9 6Macaca nemestrina 2 14 7Papio cynocephalus 2 8 6Papio anubis 2 12 9Kasi vetulus 3 9 14Semnopithecus entellus 3 30 8Trachypithecus francoisi 3 2 9Trachypithecus cristata 3 17 14Trachypithecus obscura 3 18 36Nasalis larvatus 3 11 8Piliocolobus badius 3 11 6Colobus guereza 3 23 17

Hylobatidae Hylobates lar 2 16 9Hylobates syndactylus 3 5 7

Pongidae Pongo pygmaeus 2 8 9Hominidae Pan troglodytes 2 13 8

Gorilla gorilla 3 6 7

1 Dietary categories: 1, insects or other animal matter and (to varying degrees) fruit are main dietary staples; 2, fruit is main staple,generally supplemented by foliage; and 3, foliage and/or seeds are main staples; fruit (often unripe) may be consumed to varyingdegrees.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 193

eruption schedules of folivorous primates or of le-murs in general, we supplemented the publisheddata for these taxa with life history data inferredfrom unpublished museum and captive-animalrecords. Using specimens in museum collections inEurope, the United States, and Madagascar, wecompiled known ages for zoo- or facility-raised indi-viduals (whenever available), collection dates forwild-caught lemurs (whose reproductive synchronyallows biological age to be estimated for immatureindividuals with known death dates), coat charac-teristics for colobines and some New World monkeys(whose infant and/or juvenile coat color-changeschedule allows age to be estimated for immatureindividuals with associated skins), and body massesof wild-caught and captive individuals belonging tospecies whose growth trajectories (mass increaseover time) have been published. Also consideredwere the cranial dimensions of individuals of knownages. Combining these data with previously pub-lished data on dental eruption schedules, we wereable to reconstruct at least partial dental eruptionschedules for the primate species in our database(including 10 lemur species and 8 colobines).

Life history data (age at weaning, age at firstfemale breeding, adult female body mass, adult fe-male cranial capacity) were compiled from the pri-mary literature. (Additional life history data com-piled for the same set of species were included inmultiple regression and principal components anal-yses reported elsewhere; Godfrey et al., in press, b).When values for adult female cranial capacity wereunavailable, they were measured directly from mu-seum specimens by one of the authors (W.L.J.).Adult female cranial capacities were used for allsexually dimorphic species and preferred for all spe-cies, although pooled-sex cranial capacities wereused for some sexually monomorphic species, whennecessary.

For each individual in our database, we measuredthe mesiodistal and buccolingual diameters of themilk and permanent postcanine teeth. We then cal-culated species mean values for the adult postcanineocclusal area, as well as postcanine occlusal areas attwo absolute ages (4 months and 1 year) and atweaning. Dental precocity was ascertained by count-ing the postcanine teeth erupted at 4 months, 1 year,and weaning (including the already-replaced milkteeth), and then constructing a ratio of postcanineteeth erupted at each age (or life-history stage) tothe species-typical total number of postcanine teeth(deciduous plus permanent). Endowment at weaningwas calculated by summing the average mesiodistaltimes buccolingual dimensions of all teeth present atweaning (excluding those already replaced), and cal-culating the ratio of postcanine occlusal area atweaning to the mean adult postcanine occlusal area(permanent teeth only). Dental precocity at 4months and 1 year was used to assess how absoluterates of dental development vary independently ofthe degree of dental development at weaning. Ap-

pendix A provides our dental eruption data and keylife history parameters. Appendix B lists the sourcesfor these data.

Dietary categories (insectivore, frugivore, folivore)were assigned on the basis of information in theprimary literature, and diet was treated as a cate-gorical variable (Table 1). A score of 1 (little or nofoliage) was given to species consuming primarilyinsects and fruit (“insectivores”). A score of 2 (mod-erate foliage and fiber) was given to species whoseprimary staple is fruit supplemented by leaves (“fru-givores”). A score of 3 (high foliage and fiber) wasgiven to species whose primary staple is foliage and,to varying degrees, seeds (“folivores”). All anatomi-cal or physiological as well as behavioral folivoreswere assigned to the latter category. Anatomicalfolivores consume fruit to varying degrees; fibrous,unripe fruit may be preferred over ripe fruit, andseeds are often chewed rather than swallowed wholeor discarded. The diets of many primate species areaffected by food availability and can change sub-stantially between seasons or localities. Thus, de-spite the fact that colobus and leaf monkeys are allanatomical folivores, leaf consumption at differentforests or in different seasons can vary from 47–82%(Piliocolobus badius), 47–77% (Colobus guereza),27–51% (Colobus angolensis), and so on (see Kirk-patrick, 1999). Foliage can comprise as little as 26%or as much as 94% of the diets of colobine species,and seeds can comprise as little as 0% or as much as50% (Kirkpatrick, 1999). Conversely, anatomicalfrugivores sometimes consume enormous quantitiesof leaves. Living in the dry deciduous forests of west-ern Madagascar, the western rufous lemur (Eule-mur fulvus rufus) deviates markedly from the east-ern rufous lemur (also E. f. rufus) and from all otherEulemur species, in consuming between 50–90%leaves (Sussman, 1974; Freed, 1999). In contrast,fruit makes up more than 65% of the diet of easternrufous lemurs at all times, and foliage never exceeds20% (Overdorff, 1993). Like other lemurids, E. f.rufus is not a seed predator (Overdorff and Strait,1998). Future analyses of diet and life history vari-ation should take into consideration such dietaryplasticity.

Data analysis

Our first task was to specify the predictions ofeach of our hypotheses, identifying shared as well asunique predictions. Shared and unique contribu-tions of explanatory variables were then exploredusing correlation and partial correlation analysis.Partial correlations are a convenient way to accom-plish essentially the same goal as multiple regres-sion with more than one independent variable(Smith, 1999, and references therein). For example,we can ask if body mass variation explains a signif-icant amount of variation in dental precocity aboveand beyond that explained by its covariation withcranial capacity; cranial capacity would be the vari-able “controlled for” in this case.

194 L.R. GODFREY ET AL.

A problem that sometimes plagues cross-speciesstudies is that of strong phylogenetic correlation(Felsenstein, 1985; Harvey and Pagel, 1991). Unlessone can assume a starburst phylogeny (a bad as-sumption for primates), species cannot be treated asindependent data points due to a nested hierarchy ofrelatedness. Closely related taxa are likely to besimilar simply because they share a common ances-try. This “phylogenetic inertia” can result in spuri-ously narrow confidence intervals and type I errors(Garland et al., 1992, 1999; Harvey and Purvis,1991; Pagel, 1992), in part because degrees of free-dom are grossly inflated (Smith, 1994). We acknowl-edge and adjust for this potentially serious problemby using the variance components approach ofSmith (1994) to calculate effective degrees of free-dom from “discounted” sample sizes. We use themaximum likelihood solution to variance compo-nents available in SAS (procedure “varcomp”). Todetermine the effective N for partial correlationanalysis, we followed the recommendation of Smith(1994), selecting the smaller of two choices: 1) theeffective N calculated for the dependent variable; or2) the mean of the effective Ns calculated for allvariables. Elsewhere, and in a context different fromthe hypothesis testing done here, we report the re-sults of multivariate treatments of phylogeneticallyindependent contrasts (PICs) derived from our den-tal and life-history data (Godfrey et al., in press, b).

We wish to note that the results of our analyses ofPICs are highly consistent with the results of thespecies-value analyses reported here.

Table 2 summarizes the predictions of each of thesix hypotheses and their corresponding statisticaltests. The statistical significance of correlationsfound in our analyses is assessed for both traditionaland phylogenetically reduced degrees of freedom.The appreciable difference between our sample Nsand the calculated discounted Ns points to a non-trivial amount of phylogenetic constraint to most ofour variables (Table 3). Working hypotheses are con-sidered “strongly” supported whenever discountedas well as traditional degrees of freedom yield sig-nificance at P , 0.05. They are considered “moder-ately” supported whenever P , 0.05 for traditional,but not discounted, degrees of freedom, and “weakly”supported when the signal is in the predicted direc-tion, but significance, even under traditional de-grees of freedom, is marginal (P , 0.1). Under othercircumstances, working hypotheses are unsup-ported. Directional hypotheses (e.g., A . B) aretested using one-tailed probabilities and null hy-potheses of the form A # B. When, occasionally,working hypotheses generate predictions in the formof nondirectional null hypotheses (A 5 B), they aretested using two-tailed probabilities. Whereas therationales of alternative dietary hypotheses differ,some of their predictions are shared. It is the unique

TABLE 2. Predictions of the competing hypotheses1

Prediction and hypothesis DCH BPH FIH RAH FPH PRH

Adult / mass is negatively correlated with pace of dental development, evenafter controlling for effects of cranial capacity.

X

Adult / cranial capacity is negatively correlated with absolute pace of dentaldevelopment, even after controlling for effects of body size.

X

Big-bodied species have weanlings that are less dentally advanced than thoseof small-bodied species.

X2

Big-brained species have weanlings that are less dentally advanced thanthose of small-brained species.

X3

Folivores exhibit faster dental development than do like-sized frugivores. X4 X X4 XFolivores wean their offspring earlier than do like-sized frugivores. X X XFolivores reproductively mature earlier than do like-sized frugivores. X X XFolivores exhibit more advanced dental development at weaning than do like-

sized frugivores.X X

Big-brained species have weanlings that are less dentally advanced thanthose of small-brained species, controlling for effects of body size.

X

Folivores have smaller brains than do like-sized frugivores. XThere is no difference between dental development at weaning of folivores

and frugivores, controlling for cranial capacity and body size.X

Late maturers exhibit slower dental development than like-sized earlymaturers.

X

Folivores exhibit faster dental development than do frugivores of similarbrain size.

X

Folivores exhibit more advanced dental development at weaning than dofrugivores, controlling for effects of age at weaning.

X

Folivores exhibit more advanced dental development at weaning than dofrugivores, controlling for effects of brain size.

X

Insectivores wean their offspring earlier than do like-sized frugivores. XInsectivores exhibit faster dental development than do like-sized frugivores. XInsectivores reproductively mature earlier than do like-sized frugivores. X

1 DCH, design constraint hypothesis; BPH, brain pleiotropy hypothesis; FIH, foraging independence hypothesis; RAH, risk aversionhypothesis; FPH, food processing hypothesis; PRH, protein richness hypothesis.2 Assuming weanlings of smaller-bodied species are relatively large.3 Assuming weanlings of smaller-brained species are relatively large.4 Assuming folivores wean at the same age or earlier than do like-sized frugivores.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 195

predictions of each hypothesis that are most criticalto hypothesis testing.

HYPOTHESES

The design constraint hypothesis (DCH)

The design constraint hypothesis is grounded inthe work of Taylor (1965), Western (1979), and othertheorists who treated body size as development’sengine. Its premise is that selection for changes inbody mass will effect concomitant changes in lifehistory parameters. In general, large-bodied speciesdevelop more slowly than small-bodied species (Pe-ters, 1983; Calder, 1984). If dental development is amere part and parcel of a size-driven developmentalclock, then large-bodied species should also exhibitslow dental development. Adult mass should be neg-atively correlated with the pace of dental develop-ment, even after the effects of other variables suchas cranial capacity are controlled. Furthermore, ifadult body size is the primary determinant of thepace of dental development, then, regardless of diet,species that are small should exhibit high dentalprecocity at 4 months and 1 year. Diet should havelittle or no size-independent effect on dental devel-opment. Folivores might be expected to exhibitslower dental development than frugivores, and in-sectivores faster dental development than frugi-vores, but only to the extent that folivores tend to belarger and insectivores smaller in body size.

The implications of the DCH for dental develop-ment at weaning depend on the relationship be-tween weanling and maternal mass. Implicit in thework of Taylor (1965) is the notion that all life his-tory events are scaled functions of body size. Char-nov (1991, 1993) argued that weaning occurs whenyoungsters attain a fixed proportion of maternalbody size. However, Purvis and Harvey (1995) foundthat small-bodied ungulates and other mammalstend to have weanlings that are relatively large, andthe ratio of weanling to maternal mass is inverselycorrelated with maternal mass. Whereas some haveclaimed that Charnov’s fixed-proportionality ruleholds for anthropoid primates, we found that thegeneralization by Purvis and Harvey (1995) appliesboth for anthropoids alone and for anthropoids and

strepsirrhines combined.1 Because small-bodied pri-mates tend to wean their offspring at an advancedstate of growth and development, one might expecthigh dental precocity in the weanlings of small-bod-ied species.

The brain pleiotropy hypothesis (BPH)

A central role for the brain in mammalian growthand development has been defended by many re-searchers (reviewed in Ross and Jones, 1999). Inmammals, lactation acts as a kind of buffer, protect-ing infants against the vicissitudes of the environ-ment. Virtually all postnatal brain growth is com-plete at weaning (Martin, 1983). Species with largebrains must extend the period of brain growth anddelay weaning in order to accommodate the highenergetic costs of growing large brains. The mater-nal energy hypothesis of Martin (1996) elaboratesfurther on the notion that brain growth is central toreproduction: it is the mother’s need to sustain braingrowth (via lactation) which effectively sets the de-velopmental clock (see also Lee, 1999). Cranial ca-pacity should predict age at weaning and first breed-ing. Smith (1989, 1992) argued for a link betweenbrain and dental development. Dental developmentmay be prolonged as an incidental effect of pro-longed brain growth.

If dental development is more closely tied to cra-nial capacity than to body size, then one shouldexpect, even after controlling for the effects of bodysize, that small-brained species will develop morerapidly than large-brained creatures. Adult femalecranial capacity should be inversely correlated withdental precocity at 4 months and 1 year. Becausesmall-brained species should also wean their off-spring at an early age, there is no necessary, logicalconnection between brain size and dental precocityor endowment at weaning. However, if weaning oc-curs at a relatively advanced stage of skeletal

1On the basis of anthropoid data published by Lee et al. (1991), wefound that the log10 of the ratio of weaning to maternal mass inprimates is indeed inversely correlated with log10 maternal mass (r 520.54, N 5 30, one-tailed P , 0.001). The relationship is even stron-ger when data for four lemurids and one indrid are included (r 520.60, N 5 35, one-tailed P , 0.0001). Data from the Duke UniversityPrimate Center.

TABLE 3. Effective or discounted sample sizes (after Smith, 1994)

VariableAll taxa(N 5 40)

Frugivores and folivores(N 5 35)

Insectivores and frugivores(N 5 22)

Log10 adult female mass 12 10 10Log10 adult cranial capacity 10 8 9Foliage consumption 21 26 13Age at weaning 11 9 9Age at first breeding 11 9 9Dental precocity at 4 months 9 8 6Dental precocity at 1 year 11 8 11Dental precocity at weaning 18 18 10Dental endowment at weaning 22 21 9

196 L.R. GODFREY ET AL.

growth and development in small-brained creatures,then weanlings of small species might also be ex-pected to exhibit an advanced state of dental devel-opment. Again, diet should have little or no size-independent effect on dental development. Folivoresmight be expected to exhibit more rapid dental de-velopment than like-sized frugivores, but only to theextent that they tend to have smaller brains.

The foraging independence hypothesis (FIH)

Our “foraging independence hypothesis” is a logi-cal derivative of what has been called the “need tolearn” hypothesis (Ross and Jones, 1999), anotherhypothesis which purports to explain the observedcorrelation between large brain size and delayedreproduction. Its premise is that both large brainsand late reproduction result from selection for pro-longed learning (Gibson, 1986; Dunbar, 1992, 1995;Byrne, 1995; Joffe, 1997). Whether selection oper-ates mainly to enhance social cognition or to en-hance problem-solving in complex environments, acomplex foraging support network for weanlings(with intergenerational transmission of particularforaging skills) may be options only for taxa withlarge brains. The trade-off is that, to sustain thesocial transmission of complex skills, highly enceph-alized species must also limit the number of off-spring, delay weaning, extend juvenescence, and de-lay reproduction. Youngsters acquire foraging skillsover an extended period of time, and inefficientweanlings can still survive with help from adults.This help comes in a variety of forms. Adults can setan example, engage in active pedagogy, defend foodresources against conspecifics, or transfer food di-rectly to immature individuals (Fragaszy and Bard,1997).

For weanlings of poorly encephalized species, sur-vival depends on greater self-sufficiency. Greaterdental development at weaning may compensate fora weak foraging-support network or for poor dis-crimination in food selection by weanlings. Thus,high dental precocity and endowment at weaningmay be selectively advantageous for species withrelatively low levels of peri- and postweaning mater-nal investment and weak foraging-support net-works.

The foraging independence hypothesis yields anumber of predictions, only three of which areunique to it alone (see Table 2). The unique predic-tions of the FIH are: 1) highly encephalized speciesshould have weanlings that are less advanced den-tally than those of poorly encephalized species (i.e.,controlling for the effects of body size, cranial capac-ity should be negatively correlated with dental de-velopment at weaning); 2) because they do not needto acquire complex foraging skills, folivores shouldhave smaller brains than like-sized frugivores; and3) folivores should exhibit greater dental precocityand endowment at weaning than like-sized frugi-vores only to the extent that they have relativelysmaller brains and less complex social interactions.

There is no reason to expect any differences betweenthe dental precocities of folivores and frugivores atweaning once the effects of both cranial capacity andbody size have been controlled. Predictions commonto this and some other hypotheses are: 1) if weaningis early and if dental development at weaning ismore advanced in folivores than in like-sized frugi-vores, then dental development should be morerapid (on an absolute scale) in folivores than inlike-sized frugivores; 2) because they do not need asextended a period of time to learn foraging skills,folivores should wean their offspring earlier thanlike-sized frugivores; 3) given the shorter period re-quired for skill acquisition in folivores, folivoresshould exhibit earlier reproductive maturation thanlike-sized frugivores; and finally, 4) due to thesmaller group sizes and less complex social interac-tions of folivores, newly weaned folivores should bemore advanced dentally than newly weaned, like-sized frugivores.

The risk aversion hypothesis (RAH)

The premise of the risk aversion hypothesis is thatresource distribution and abundance covary withdiet, and affect the risk of starvation (Janson andvan Schaik, 1993; Leigh, 1994). Due to higher in-traspecific competition for scarce resources, juve-niles living in risky environments will be more likelyto die of starvation than juveniles living in low-riskenvironments. Slower growth reduces the probabil-ity of starvation, and is therefore favored by selec-tion for species exploiting risky food resources.

Some researchers have noted that the RAH ishard to test because the degree to which resourcesare actually limiting is often difficult to measure(Watts and Pusey, 1993). However, Leigh (1994)defended the RAH, using broad comparisons of fo-livorous and frugivorous anthropoids, on the explicitpresumption that the foods exploited by frugivoresare riskier than those eaten by folivores (Janson andvan Schaik, 1993). Leigh (1994) used growth curvesto test this hypothesis; the predictions of the RAHfor dental development were not tested. The soleunique prediction of the RAH is that the absoluterate of dental development should be inversely cor-related with age at first breeding; late maturersshould develop slowly (Table 2). In addition, if thekey to reduced predation mortality is rapid growthand maturation, folivores might be expected to weantheir young at an earlier age, and to mature earlierthan species relying on less predictable food re-sources. Rapid dental development should charac-terize folivores, but there is no reason to expectadvanced dental development at weaning, becausedental precocity at weaning is not the target of se-lection, and because weaning should also be early.

The food processing hypothesis (FPH)

The premise of the food processing hypothesis isthat the mechanical requirements of mastication co-

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 197

vary with diet. According to this hypothesis, selec-tion must prepare weanlings to process those solidfoods available to them at weaning or shortly there-after (Eaglen, 1985). Dental endowment and precoc-ity at weaning will therefore depend on the mechan-ical requirements for processing those foods. Thishypothesis predicts that dental development atweaning is directly targeted by selection. Folivorousweanlings need to be better equipped than frugivo-rous weanlings, not only because they must breakdown highly fibrous sheetlike foods, but becausethey tend to masticate (rather than discard or swal-low whole) seeds (Dew and Wright, 1998; Heming-way, 1996, 1998; Kirkpatrick, 1999; Overdorff andStrait, 1998). Differences in the morphology of thepermanent cheek teeth of folivores and frugivoreshave been studied in detail (Covert, 1986; Jungers etal., in press; Kay, 1978; Yamashita, 1998a,b). Foli-vores have molars with relatively higher and longershearing blades and larger crushing basins.

The FPH predicts that diet directly influencesdentition at weaning. This influence should be inde-pendent of age at weaning, brain size, or body size.Unless age at weaning is delayed in folivores, thedentitions of folivores and seed predators might beexpected to develop faster (on an absolute scale)than those of frugivores. Thus, folivores might beexpected to exhibit faster dental development thanfrugivores of similar body size. The unique predic-tions of the FPH are that: 1) folivores should exhibitfaster dental development on an absolute scale thanfrugivores of similar brain size; 2) with age at wean-ing controlled, folivores should exhibit more ad-vanced dental development at weaning than frugi-vores; and 3) with brain size controlled, folivoresshould exhibit more advanced dental developmentat weaning than frugivores.

The protein richness hypothesis (PRH)

The premise of the protein richness hypothesis isthat, because protein is essential for growth, therelative amount of protein in the diet influencesrates of growth and development (Glander, 1980;Froehlich et al., 1981). Species with diets high inprotein should experience rapid dental eruption as acorollary of rapid overall growth and maturation.Leaves, seeds, and insects are high in protein, andmight facilitate rapid growth. A caveat is that themain staple in the diet is not necessarily a goodindicator of the quality of the diet. As Wright (1999)notes, whereas anthropoid folivore milk is higher inprotein content than that of anthropoid frugivores,the same is not the case for folivorous vs. frugivorouslemurs.

If protein consumption is the primary determi-nant of rate of development, then folivores, seedpredators, and insectivores might be expected todevelop and mature more rapidly than frugivores ofcomparable adult body size. This hypothesis makesno prediction regarding dental development atweaning, but it does predict early weaning and first

TA

BL

E4.

Tes

tof

des

ign

con

stra

int

and

brai

npl

eiot

ropy

hyp

oth

eses

,w

ith

effe

ctiv

eN

san

dpr

obab

ilit

ies

un

der

dis

cou

nti

ng

inpa

ren

thes

es1

Wor

kin

gh

ypot

hes

isP

redi

ctio

ns

ofw

orki

ng

hyp

oth

esis

Dep

ende

nt

vari

able

Exp

lan

ator

yva

riab

leC

ontr

olle

dva

riab

ler

orpa

rtia

lr

N(N

eff.

)

Tes

tof

nu

llh

ypot

hes

isw

ith

Pva

lues

Wor

kin

gh

ypot

hes

issu

ppor

ted?

DC

HA

dult

/m

ass

isn

egat

ivel

yco

rrel

ated

wit

hpa

ceof

den

tal

deve

lopm

ent,

even

afte

rco

ntr

olli

ng

for

effe

cts

ofcr

ania

lca

paci

ty.

Den

tal

prec

ocit

yat

4m

onth

sL

ogad

ult

/m

ass

Log

cran

ial

capa

city

0.52

40(9

)0.

999

(0.9

21)

No

Den

tal

prec

ocit

yat

1ye

arL

ogad

ult

/m

ass

Log

cran

ial

capa

city

0.43

40(1

1)0.

997

(0.9

03)

No

Big

-bod

ied

spec

ies

hav

ew

ean

lin

gsth

atar

ele

ssde

nta

lly

adva

nce

dth

anw

ean

lin

gsof

smal

l-bo

died

spec

ies.

Den

tal

prec

ocit

yat

wea

nin

gL

ogad

ult

/m

ass

20.

1740

(14)

0.14

7(0

.276

)N

o

BP

HA

dult

/cr

ania

lca

paci

tyis

neg

ativ

ely

corr

elat

edw

ith

pace

ofde

nta

lde

velo

pmen

t,ev

enaf

ter

con

trol

lin

gfo

ref

fect

sof

body

size

.

Den

tal

prec

ocit

yat

4m

onth

sL

ogcr

ania

lca

paci

tyL

ogad

ult

/m

ass

20.

7740

(9)

0.00

0(0

.006

)Y

es,

stro

ngl

y

Den

tal

prec

ocit

yat

1ye

arL

ogcr

ania

lca

paci

tyL

ogad

ult

/m

ass

20.

6940

(11)

0.00

0(0

.008

)Y

es,

stro

ngl

y

Big

-bra

ined

spec

ies

hav

ew

ean

lin

gsth

atar

ele

ssde

nta

lly

adva

nce

dth

anw

ean

lin

gsof

smal

l-br

ain

edsp

ecie

s.

Den

tal

prec

ocit

yat

wea

nin

gL

ogcr

ania

lca

paci

ty2

0.31

40(1

4)0.

025

(0.1

33)

Yes

,m

oder

atel

y

1D

CH

,de

sign

con

stra

int

hyp

oth

esis

;B

PH

,br

ain

plei

otro

pyh

ypot

hes

is.

198 L.R. GODFREY ET AL.

TA

BL

E5.

Tes

tfo

rth

efo

ragi

ng

ind

epen

den

ceh

ypot

hes

is(u

niq

ue

pred

icti

ons

inbo

ld)

Pre

dict

ion

sof

wor

kin

gh

ypot

hes

isD

epen

den

tva

riab

leE

xpla

nat

ory

vari

able

Con

trol

led

vari

able

Par

tial

rN

(Nef

f.)

Tes

tof

nu

llh

ypot

hes

isw

ith

Pva

lues

Wor

kin

gh

ypot

hes

issu

ppor

ted?

Fol

ivor

esex

hib

itfa

ster

den

tal

deve

lopm

ent

than

doli

ke-s

ized

fru

givo

res.

Den

tal

prec

ocit

yat

4m

onth

sD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.61

35(8

)0.

000

(0.0

56)

Yes

,m

oder

atel

y

Den

tal

prec

ocit

yat

1ye

arD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.50

35(8

)0.

001

(0.1

10)

Yes

,m

oder

atel

y

Fol

ivor

esw

ean

thei

rof

fspr

ing

earl

ier

than

doli

ke-s

ized

fru

givo

res.

Age

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s2

0.35

35(9

)0.

013

(0.1

85)

Yes

,m

oder

atel

y

Fol

ivor

esre

prod

uct

ivel

ym

atu

reea

rlie

rth

ando

like

-siz

edfr

ugi

vore

s.

Age

at/

firs

tbr

eedi

ng

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s2

0.32

35(9

)0.

030

(0.2

08)

Yes

,m

oder

atel

y

Fol

ivor

esex

hib

itm

ore

adva

nce

dde

nta

lde

velo

pmen

tat

wea

nin

gth

ando

like

-siz

edfr

ugi

vore

s.

Den

tal

prec

ocit

yat

wea

nin

gD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.45

35(1

8)0.

003

(0.0

30)

Yes

,st

ron

gly

Den

tal

endo

wm

ent

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s0.

3235

(19)

0.00

0(0

.092

)Y

es,

mod

erat

ely

Big

-bra

ined

spec

ies

hav

ele

ssad

van

ced

wea

nli

ngs

than

smal

l-b

rain

edsp

ecie

s,co

ntr

olli

ng

for

effe

cts

ofb

ody

size

.

Den

tal

pre

coci

tyat

wea

nin

gL

ogcr

ania

lca

pac

ity

Log

adu

lt/

mas

s2

0.52

40(1

3.33

)0.

000

(0.0

32)

Yes

,str

ongl

y

Den

tal

end

owm

ent

atw

ean

ing

Log

cran

ial

cap

acit

yL

ogad

ult

/m

ass

20.

3140

(14.

67)

0.02

5(0

.137

)Y

es,m

oder

atel

y

Fol

ivor

esh

ave

smal

ler

bra

ins

than

do

lik

e-si

zed

fru

givo

res.

Log

adu

lt/

cran

ial

cap

acit

yD

iet:

fru

givo

res

vs.f

oliv

ores

Log

adu

lt/

mas

s2

0.66

35(8

)0.

000

(0.0

38)

Yes

,str

ongl

y

Fol

ivor

esan

dfr

ugi

vore

sex

hib

itn

od

iffe

ren

cein

den

tal

dev

elop

men

tat

wea

nin

g,w

hen

effe

cts

ofb

oth

cran

ial

cap

acit

yan

db

ody

size

are

con

trol

led

(tes

tis

two-

tail

ed).

Den

tal

pre

coci

tyat

wea

nin

gD

iet:

fru

givo

res

vs.f

oliv

ores

Log

adu

lt/

mas

san

dlo

gcr

ania

lca

pac

ity

0.14

35(1

5.5)

0.43

4(0

.633

)Y

es,c

ann

otre

ject

nu

llh

ypot

hes

is

Den

tal

end

owm

ent

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fol

ivor

esL

ogad

ult

/m

ass

and

log

cran

ial

cap

acit

y

0.10

35(1

6.25

)0.

578

(0.7

26)

Yes

,can

not

reje

ctn

ull

hyp

oth

esis

breeding in species with high protein diets (oncebody size is controlled). Its unique predictions per-tain to comparisons between insectivores and frugi-vores (Table 2).

RESULTS

Let us consider each of our hypotheses in light ofour data. The brain pleiotropy hypothesis does con-siderably better than the design constraint hypoth-esis at explaining variation in dental developmentamong primates (Table 4). Adult body size farespoorly in comparison to cranial capacity when usedto predict the pace of dental development. It is onlybecause adult body mass is correlated with othertraits (cranial capacity) that are more stronglylinked to dental development that it predicts thepace of dental development at all. Cranial capacityis the best predictor of dental precocity at 4 monthsand 1 year, as anticipated by Smith et al. (1994).

The shared predictions of the four dietary hypoth-eses tend to be moderately or strongly supported(Tables 5–8). The unique predictions of the foragingindependence hypothesis are also well supported bythe data (Table 5). They are that folivores havesmaller brains than like-sized frugivores, and that,once the effects of both cranial capacity and bodysize have been removed, there will be no differencebetween the dentitions of folivores and frugivores atweaning. Lemurs comprise an apparent exception tothe latter rule, however. Folivorous lemurs exhibitgreater precocity at weaning than do frugivorouslemurs, even after controlling for both brain andbody size (partial correlation 5 0.69, one-tailed P 50.019, N 5 10). This sample is too small to undergomeaningful discounting.

The unique predictions of the risk aversion hy-pothesis are not supported by our data (Table 6).There is little or no connection between age at firstbreeding and the pace of dental development, oncethe effects of body size are controlled. The predictedlink between the pace of reproductive and ecological(dental) maturation is not supported by our data.Furthermore, the RAH cannot account for the ob-served high dental precocity and endowment of foli-vores at weaning. Clearly, dental developmental ac-celeration is not solely part and parcel of a generalacceleration of growth and development in folivores.

The food processing hypothesis, that the mechan-ical requirements for food processing affect dentaldevelopment at weaning, is well supported by ourdata (Table 7). Folivorous weanlings tend to havehigh dental precocity and endowment, particularlywhen compared to like-sized, more frugivorous rel-atives. The unique predictions of the FPH (first, thatfolivore/seed predators will exhibit faster dental de-velopment than frugivores of similar brain size; andsecond, that with age at weaning controlled, folivore/seed predators will exhibit more advanced dentaldevelopment at weaning) are supported by our data.

The protein richness hypothesis, that the pace ofdevelopment depends on the amount of protein in

TA

BL

E6.

Tes

tof

the

risk

aver

sion

hyp

oth

esis

(un

iqu

epr

edic

tion

sin

bold

)

Pre

dict

ion

sof

wor

kin

gh

ypot

hes

isD

epen

den

tva

riab

leE

xpla

nat

ory

vari

able

Con

trol

led

vari

able

Par

tial

rN

(Nef

f.)

Tes

tof

nu

llh

ypot

hes

isw

ith

Pva

lues

Wor

kin

gh

ypot

hes

issu

ppor

ted?

Fol

ivor

esex

hib

itfa

ster

den

tal

deve

lopm

ent

than

doli

ke-s

ized

fru

givo

res.

Den

tal

prec

ocit

yat

4m

onth

sD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.61

35(8

)0.

000

(0.0

56)

Yes

,m

oder

atel

y

Den

tal

prec

ocit

yat

1ye

arD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.50

35(8

)0.

001

(0.1

10)

Yes

,m

oder

atel

y

Fol

ivor

esw

ean

thei

rof

fspr

ing

earl

ier

than

like

-si

zed

fru

givo

res.

Age

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s2

0.35

35(9

)0.

013

(0.1

85)

Yes

,m

oder

atel

y

Fol

ivor

esre

prod

uct

ivel

ym

atu

reea

rlie

rth

anli

ke-s

ized

fru

givo

res.

Age

atfi

rst

bree

din

gD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

20.

3235

(9)

0.03

0(0

.208

)Y

es,

mod

erat

ely

Lat

em

atu

rers

exh

ibit

slow

er(d

enta

l)d

evel

opm

ent

than

lik

e-si

zed

earl

ym

atu

rers

.

Den

tal

pre

coci

tyat

4m

onth

sA

geat

firs

tb

reed

ing

Log

adu

lt/

mas

s2

0.14

40(9

)0.

195

(0.3

65)

No

Den

tal

pre

coci

tyat

1ye

arA

geat

firs

tb

reed

ing

Log

adu

lt/

mas

s0.

0940

(11)

0.29

2(0

.362

)N

o

200 L.R. GODFREY ET AL.

TA

BL

E7.

Tes

tof

food

proc

essi

ng

hyp

oth

esis

(un

iqu

epr

edic

tion

sin

bold

)

Pre

dict

ion

sof

wor

kin

gh

ypot

hes

isD

epen

den

tva

riab

leE

xpla

nat

ory

vari

able

Con

trol

led

vari

able

Par

tial

rN

(Nef

f.)

Tes

tof

nu

llh

ypot

hes

isw

ith

Pva

lues

Wor

kin

gh

ypot

hes

issu

ppor

ted?

Fol

ivor

esex

hib

itfa

ster

den

tal

deve

lopm

ent

than

doli

ke-s

ized

fru

givo

res.

Den

tal

prec

ocit

yat

4m

onth

sD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.61

35(8

)0.

000

(0.0

56)

Yes

,m

oder

atel

y

Den

tal

prec

ocit

yat

1ye

arD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.50

35(8

)0.

001

(0.1

10)

Yes

,m

oder

atel

y

Fol

ivor

esex

hib

itm

ore

adva

nce

dde

nta

lde

velo

pmen

tat

wea

nin

gth

ando

like

-siz

edfr

ugi

vore

s.

Den

tal

prec

ocit

yat

wea

nin

gD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.45

35(1

8)0.

003

(0.0

30)

Yes

,st

ron

gly

Den

tal

endo

wm

ent

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s0.

3235

(19)

0.00

0(0

.092

)Y

es,

mod

erat

ely

Fol

ivor

esex

hib

itfa

ster

den

tal

dev

elop

men

tth

and

ofr

ugi

vore

sof

sim

ilar

bra

insi

ze.

Den

tal

pre

coci

tyat

4m

onth

sD

iet:

fru

givo

res

vs.f

oliv

ores

Log

cran

ial

cap

acit

y0.

4635

(8)

0.00

3(0

.133

)Y

es,m

oder

atel

y

Den

tal

pre

coci

tyat

1ye

arD

iet:

fru

givo

res

vs.f

oliv

ores

Log

cran

ial

cap

acit

y0.

3635

(8)

0.01

7(0

.200

)Y

es,m

oder

atel

y

Fol

ivor

esex

hib

itm

ore

adva

nce

dd

enta

ld

evel

opm

ent

atw

ean

ing

than

do

fru

givo

res,

con

trol

lin

gfo

rag

eat

wea

nin

g.

Den

tal

pre

coci

tyat

wea

nin

gD

iet:

fru

givo

res

vs.f

oliv

ores

Age

atw

ean

ing

0.46

35(1

7.67

)0.

003

(0.0

29)

Yes

,str

ongl

y

Den

tal

end

owm

ent

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fol

ivor

es

Age

atw

ean

ing

0.33

35(1

8.67

)0.

026

(0.0

88)

Yes

,mod

erat

ely

Fol

ivor

esex

hib

itm

ore

adva

nce

dd

enta

ld

evel

opm

ent

atw

ean

ing

than

do

fru

givo

res

ofsi

mil

arb

rain

size

.

Den

tal

pre

coci

tyat

wea

nin

gD

iet:

fru

givo

res

vs.f

oliv

ores

Log

cran

ial

cap

acit

y0.

4135

(17.

33)

0.00

7(0

.049

)Y

es,s

tron

gly

Den

tal

end

owm

ent

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fol

ivor

es

Log

cran

ial

cap

acit

y0.

2635

(18.

33)

0.06

6(0

.149

)Y

es,w

eak

ly

the diet, receives mixed support (Table 8). On theone hand, it is generally true that species feeding onlarge amounts of insects, seeds, or foliage developquickly. However, these species are also typicallyeither small-bodied or small-brained. The uniquepredictions of the PRH are poorly supported by ourdata. Against expectations, controlling for the ef-fects of body size, insectivores do not wean theiroffspring earlier than frugivores. Also against expec-tations, controlling for body size, there is no indica-tion that insectivores mature earlier than frugi-vores. The prediction that insectivores shouldexhibit faster dental development (on an absolutescale) than “like-sized” frugivores receives equivocalsupport.

An important consideration is the special role ofage at weaning. Whereas age at weaning is betterpredicted by brain than by body size, it remainssignificantly correlated with age at first breeding,even after the effects of both log brain and log bodysize are controlled.2 It appears that selection caneffect changes in the timing of reproductive eventsthat are independent of size. It can also alter theplasticity of reproductive timing. In some species,weaning is sharply constrained phenologically (relemurs, see Sauther, 1991; Wright, 1997, 1999). Inothers, weaning is far less constrained. A case inpoint is Pongo pygmaeus. Its “age at weaning” hasbeen reported as 1.12 years (Ross and Jones, 1999),3.5 years (Lee, 1999), and between 6–8 years(Markham, 1994). Even when “weaning” is preciselydefined as the transition from life-sustaining to in-cidental dependency on the mother, its timing can beplastic (discussed in Lee, 1966, 1999). Weaning andreproductive maturation are affected by extrinsicvariables (such as predation, available resources,climate; see Wolfe, 1986; Boinski, 1987; Lee et al.,1991; Lee, 1996) as well as the intrinsic variables(such as brain and body size) that we have beenexploring here.

As might be expected (given the positive correla-tion between age at weaning and brain or body size,and the negative correlation between age at wean-ing and the pace of dental development), the ratio ofdental development at weaning to age at weaningcovaries inversely with brain and body size in pri-mates (Fig. 1). Its correlation with cranial capacityis far tighter than that with body size. What is ofinterest to us here is the tendency for folivores indiverse clades to exhibit higher values for this ratio

2Partial correlation 5 0.88, N 5 40, one-tailed P , 0.0001 with 36degrees of freedom; Neff. 5 11, P , 0.001 with 7 degrees of freedom.

Fig. 1. a: Scatterplot of log10 (dental precocity at weaning/age atweaning) vs. log10 (adult female mass). Triangles are insectivores,squares are frugivores, and circles are folivores (solid circles areIndridae). b: Scatterplot of log10 (dental precocity at weaning/age atweaning) vs. log10 (adult female cranial capacity). Triangles are in-sectivores, squares are frugivores, and circles are folivores (solid cir-cles are Indridae).

TA

BL

E8.

Tes

tof

prot

ein

rich

nes

sh

ypot

hes

is(u

niq

ue

pred

icti

ons

inbo

ld)

Pre

dict

ion

sof

wor

kin

gh

ypot

hes

isD

epen

den

tva

riab

leE

xpla

nat

ory

vari

able

Con

trol

led

vari

able

Par

tial

rN

(Nef

f.)

Tes

tof

nu

llh

ypot

hes

isw

ith

Pva

lues

Wor

kin

gh

ypot

hes

issu

ppor

ted?

Fol

ivor

esex

hib

itfa

ster

den

tal

deve

lopm

ent

than

doli

ke-s

ized

fru

givo

res.

Den

tal

prec

ocit

yat

4m

onth

sD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.61

35(8

)0.

000

(0.0

56)

Yes

,m

oder

atel

y

Den

tal

prec

ocit

yat

1ye

arD

iet:

fru

givo

res

vs.

foli

vore

sL

ogad

ult

/m

ass

0.50

35(8

)0.

001

(0.1

10)

Yes

,m

oder

atel

y

Fol

ivor

esw

ean

thei

rof

fspr

ing

earl

ier

than

doli

ke-s

ized

fru

givo

res.

Age

atw

ean

ing

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s2

0.35

35(9

)0.

013

(0.1

85)

Yes

,m

oder

atel

y

Fol

ivor

esre

prod

uct

ivel

ym

atu

reea

rlie

rth

ando

like

-siz

edfr

ugi

vore

s.A

geat

firs

tbr

eedi

ng

Die

t:fr

ugi

vore

svs

.fo

livo

res

Log

adu

lt/

mas

s2

0.32

35(9

)0.

030

(0.2

08)

Yes

,m

oder

atel

y

Inse

ctiv

ores

wea

nth

eir

offs

pri

ng

earl

ier

than

do

lik

e-si

zed

fru

givo

res.

Age

atw

ean

ing

Die

t:in

sect

ivor

esvs

.fru

givo

res

Log

adu

lt/

mas

s2

0.54

22(9

)0.

996

(0.9

31)

No

Inse

ctiv

ores

rep

rod

uct

ivel

ym

atu

reea

rlie

rth

and

oli

ke-

size

dfr

ugi

vore

s.A

geat

firs

tb

reed

ing

Die

t:in

sect

ivor

esvs

.fru

givo

res

Log

adu

lt/

mas

s2

0.48

22(9

)0.

989

(0.9

00)

No

Inse

ctiv

ores

exh

ibit

fast

erd

enta

ld

evel

opm

ent

than

do

lik

e-si

zed

fru

givo

res.

Den

tal

pre

coci

tyat

4m

onth

sD

iet:

inse

ctiv

ores

vs.f

rugi

vore

sL

ogad

ult

/m

ass

20.

0322

(6)

0.55

2(0

.521

)N

o

Den

tal

pre

coci

tyat

1ye

arD

iet:

inse

ctiv

ores

vs.f

rugi

vore

sL

ogad

ult

/m

ass

20.

3822

(11)

0.04

0(0

.129

)Y

es,m

oder

atel

y

202 L.R. GODFREY ET AL.

Fig. 1.

than do closely related frugivores. This difference isnot a function of body size (Fig. 1a); and as particu-larly high positive transpositions for the leaf- andseed-eating Indridae demonstrate (Fig. 1b), it is notentirely a function of brain size.

Finally, we note that, whereas folivores tend toexhibit greater dental endowment as well as greaterprecocity at weaning than do like-sized frugivores,the signal tends to be stronger for precocity than forendowment. Because the milk dentitions of frugi-vores must be functional over a longer period oftime, and because the milk teeth of frugivores formin relatively larger jaws (due to their relatively re-tarded eruption schedule), the milk teeth of frugi-vores tend to be large. Folivores, on the other hand,tend to have relatively larger permanent molars(Kay, 1978; Godfrey et al., in press, a).

CONCLUSIONS

We examined a number of hypotheses regardingthe absolute pace of dental development, i.e., thatdental development will be rapid in species thatexhibit: 1) small adult body size (design constrainthypothesis); 2) low cranial capacity (brain pleiotropyhypothesis); 3) rapid acquisition of foraging indepen-dence, coupled with low encephalization, and lowperi- and postweaning parental investment (forag-ing independence hypothesis); 4) a low risk of star-vation due to intraspecific competition for food re-sources, coupled with a relatively high risk ofjuvenile mortality due to predation (risk aversionhypothesis); 5) a diet that is high in fibrous leafymaterial and/or seeds, and requiring extensive pro-cessing (food processing hypothesis); and 6) a dietthat is rich in protein (protein richness hypothesis).Several of these hypotheses also predict high dentalendowment and precocity in folivores at weaning.They thus converge in predicting accelerated dentaldevelopment in folivores on both absolute and rela-tive scales. Our data show that brain size is a betterpredictor of dental development than body size.However, they also affirm the insufficiency of cranialcapacity as a predictor of dental development; thecomplexity of the absolute and relative pace of den-tal development in primates is more than any singlefactor can bear.

In particular, we found that diet affects the abso-lute pace of dental development, independent ofbody size, age at first breeding, and cranial capacity.Folivores generally have more accelerated dentaldevelopmental schedules than do comparably sizedfrugivores. But their accelerated dental develop-ment is not a mere consequence of a general patternof life history acceleration in more folivorous taxa.Dental development in folivorous species also tendsto be more advanced at weaning. Neither cranialcapacity nor body size alone can account for thevariation in the absolute or relative pace of dentaleruption across all primate taxa. The advanced stateof the dentitions of folivores at weaning (with vari-ation in size and age at weaning controlled) suggests

that the state of dental development at weaning canbe the direct target of selection; the mechanics offood processing may have an important effect ondental ontogeny. In general, our data offer the stron-gest support for the foraging independence and thefood processing hypotheses, and equivocal supportfor the other dietary hypotheses. The (perhaps dif-ferent) contributions of learning, food processing,and environmental risk to dental development inmembers of diverse primate clades are certainlyworthy of future investigation.

ACKNOWLEDGMENTS

This project would not have been possible withoutthe assistance of numerous people. For help in sup-plying specimens or unpublished data, we are in-debted to David Archibald, Jacqui Bowman, G. GrayEaton, Jack Fooden, Kenneth Glander, ChristinaGrassi, David Haring, Claire Hemingway, MitchellIrwin, Karin Isler, Stephen King, Steven Leigh,Lawrence Martin, Robert Martin, Leanne Nash,Sheila O’Connor, J. Michael Plavcan, Alison Rich-ard, Elwyn Simons, Chia Tan, Michael Van Patten,and Patricia Wright. Data were compiled from therecords of and/or specimens at the following facili-ties: American Museum of Natural History, NewYork; Anthropologisches Institut und Museum, Zu-rich; Aukland Zoological Park; California PrimateResearch Center, Davis; Columbus Zoological Gar-den; Dallas Zoo; Department of Anthropology, Uni-versity of Massachusetts, Amherst; Duke UniversityPrimate Center; Field Museum of Natural History,Chicago; Hogle Zoo of Utah; Houston Zoological Gar-dens; Laboratoire de Paleontologie des Vertebres,Universite d’Antananarivo, Madagascar; Labora-toire de Zoologie, Museum National d’Histoire Na-turelle, Paris; Lowry Park; Museum of ComparativeZoology at Harvard University; Nationaal Natuur-historisch Museum, Leiden; Natural History Mu-seum, London; Oregon Regional Primate Center;Parc Ivoloina; Parc Tsimbazaza; Pittsburgh Zoo; Ra-nomafana National Park; San Diego State Univer-sity; San Diego Zoo; State University of New York atStony Brook; Smithsonian Institution; WoodlandPark Zoological Gardens; and the Yerkes RegionalPrimate Center. This research was supported inpart by NSF GER 9450175 to L.R.G., and NSF SBR-9630350 to Elwyn Simons and the Statistical Con-sulting Center of the University of Massachusetts.Special thanks are owed to the curators of collec-tions, anonymous reviewers, and Darren Godfrey,who produced Figure 1.

LITERATURE CITED

Albignac R. 1981. Variabilite dans l’organisation territoriale etl’ecologie de Avahi laniger (lemurien nocturne de Madagascar).C R Acad Sci [III] 292:331–334.

Anemone RL, Mooney MP, Siegel MI. 1996. Longitudinal study ofdental development in chimpanzees of known chronologicalage: implications for understanding age at death of Plio-Pleis-tocene hominids. Am J Phys Anthropol 99:119–133.

204 L.R. GODFREY ET AL.

Ayers JMC. 1986. Uakaris and Amazonian flooded forest. Ph.D.dissertation. University of Cambridge.

Baldwin JD. 1985. The behavior of squirrel monkeys (Saimiri) innatural environments. In: Rosenblum LA, Coe CL, editors.Handbook of squirrel monkey research. New York: PlenumPress. p 35–53.

Baldwin JD, Baldwin JI. 1981. The squirrel monkey, genusSaimiri. In: Coimbra-Filho AF, Mittermeier RA, editors. Ecol-ogy and behavior of neotropical primates, volume 1. Rio deJaneiro: Academia Brasileira de Ciencias. p 277–330.

Bauchot R, Stephan H. 1966. Donnees nouvelles sur l’encephal-isation des insectivores et des prosimiens. Mammalia 30:160–196.

Bentley-Condit VK, Smith EO. 1997. Female reproductive para-maters of Tana River yellow baboons. Int J Primatol 18:581–596.

Bernstein IS. 1968. The lutong of Kuala Selangor. Behaviour(Leiden) 32:1–16.

Boinski S. 1987. Birth synchrony in squirrel monkeys (Saimirioerstedi): a strategy to reduce neonatal predation. Behav EcolSociobiol 21:393–400.

Brandon-Jones D. 1985. Colobus and leaf monkeys. In: Mac-Donald D, editor. Primates. New York: Torstar Books. p 102–112.

Brockman DK, Willis MS, Karesh WB. 1987. Management andhusbandry of ruffed lemurs, Varecia variegata, at the San Di-ego Zoo. II. Reproduction, pregnancy, parturition, litter size,infant care and reintroduction of hand-raised infants. Zoo Biol6:343–369.

Butynski TM. 1988. Guenon birth seasons and correlates withrainfall and food. In: Gautier-Hion A, Bourliere F, Gautier JP,Kingdon J, editors. A primate radiation: evolutionary biology ofthe African guenons. Cambridge: Cambridge Univ. Press. p284–322.

Byrne RW. 1995. Primate cognition: comparing problems andskills. Am J Primatol 37:127–141.

Calder WA III. 1984. Size, function, and life history. Cambridge,MA: Harvard University Press.

Carpenter R. 1935. Behavior of the red spider monkeys in Pan-ama. J Mammal 16:171–180.

Cartmill M, Brown K, Eaglen R, Anderson DE. 1979. Hand-rearing twin ruffed lemurs Lemur variegatus at the Duke Uni-versity Primate Center. Int Zoo Yrbk 19:258–261.

Chapman C. 1987. Flexibility in diets of three species of CostaRican primates. Folia Primatol (Basel) 49:90–105.

Charnov EL. 1991. Evolution of life history variation amongfemale mammals. Proc Natl Acad Sci USA 88:1134–1137.

Charnov EL. 1993. Life history invariants: Some explorations ofsymmetry in evolutionary ecology. Oxford: Oxford UniversityPress.

Chase JE, Cooper RW. 1969. Saguinus nigricollis: physicalgrowth and dental eruption in a small population of captive-born individuals. Am J Phys Anthropol 30:111–116.

Chivers DJ, Raemaekers JJ. 1980. Long-term changes in behav-ior. In: Chivers DJ, editor. Malayan forest primates: ten years’study in tropical rain forest. New York: Plenum Press. p 209–260.

Clarke MR. 1990. Behavioral development and socialization ofinfants in a free-ranging group of howling monkeys (Alouattapalliata). Folia Primatol (Basel) 54:1–15.

Colquhoun IC. 1993. The socioecology of Eulemur macaco: a pre-liminary report. In: Kappeler PM, Ganzhorn JU, editors. Le-mur social systems and their ecological basis. New York: Ple-num. p 11–24.

Conroy G, Mahoney CJ. 1991. Mixed longitudinal study of dentalemergence in the chimpanzee, Pan troglodytes (Primates,Pongidae). Am J Phys Anthropol 86:243–254.

Covert HH. 1986. Biology of early Cenozoic primates. In: Swin-dler DR, Erwin J, editors. Comparative primate biology volume1: systematics, evolution, and anatomy. New York: A.R. Liss. p335–359.

Crandall LS. 1964. The management of wild animals in captivity.Chicago: University of Chicago Press.

Curtin SH, Chivers DJ. 1978. Leaf-eating primates of peninsularMalaysia: the siamang and the dusky leaf-monkey. In: Mont-gomery GG, editor. The ecology of arboreal folivores. Washing-ton, DC: Smithsonian Institution Press. p 441–464.

Dew JL, Wright PC. 1998. Frugivory and seed dispersal by fourspecies of primates in Madagascar’s eastern rain forest. Biotro-pica 30:425–437.

Dirks W. 1998. Histological reconstruction of dental developmentand age at death in a juvenile gibbon (Hylobates lar). J HumEvol 35:411–425.

Doyle GA. 1979. Development of behavior in prosimians withspecial reference to the lesser bushbaby, Galago senegalensismoholi. In: Doyle GA, Martin RD, editors. The study of pro-simian behavior. New York: Academic Press. p 158–206.

Dunbar RIM. 1992. Neocortex size as a constraint on group size inprimates. J Hum Evol 22:469–494.

Dunbar RIM. 1995. Neocortex size and group size in primates: atest of the hypothesis. J Hum Evol 28:287–296.

Eaglen RH. 1985. Behavioral correlates of tooth eruption inMadagascar lemurs. Am J Phys Anthropol 66:307–315.

Eisenberg JF. 1981. The mammalian radiations: an analysis oftrends in evolution, adaptation, and behavior. Chicago: Univer-sity of Chicago Press.

Eisenberg JF. 1989. Order Primates. In: Mammals of the neo-tropics. Volume 1. The northern neotropics: Panama, Colombia,Venezuela, Guyana, Suriname, French Guiana. Chicago: Uni-versity of Chicago Press. p 233–261.

Eley RM, Strum SC, Muchemi G, Reid GDF. 1989. Nutrition,body condition, activity patterns, and parasitism of free-rang-ing baboons (Papio anubis) in Kenya. Am J Primatol 18:209–219.

Ellefson JO. 1974. A natural history of white-handed gibbons inthe Malayan peninsula. In: Rumbaugh DM, editor. Gibbon andsiamang, volume 3. Basel: Karger. p 1–136.

Epple G. 1970. Maintenance, breeding and development of mar-moset monkeys (Callithricidae) in captivity. Folia Primatol(Basel) 13:48–62.

Fedigan L, Rose L. 1995. Interbirth intervals in sympatric mon-keys in Central America. Am J Primatol 15:235–245.

Felsenstein J. 1985. Phylogenies and the comparative method.Am Nat 125:1–15.

Fleagle JG. 1998. Primate adaptation and evolution, 2nd ed. NewYork: Academic Press.

Fleagle JG, Mittermeier RA. 1980. Locomotor behavior, body size,and comparative ecology of seven Surinam monkeys. Am JPhys Anthropol 52:301–314.

Fleagle JG, Schaffler M. 1982. Development and eruption of themandibular cheek-teeth in Cebus albifrons. Folia Primatol(Basel) 38:158—169.

Foerg R. 1982. Reproductive behaviour in Varecia variegata. Fo-lia Primatol (Basel) 38:108–121.

Fooden J. 1975. Taxonomy and evolution of liontail and pigtailmacaques (Primates: Cercopithecidae). Fieldiana Zool 67:1–169.

Fooden J. 1995. Systematic review of southeast Asian longtailmacaques, Macaca fascicularis (Raffles, 1821). Fieldiana ZoolNS 81:1–206.

Fooden J, Izor RJ. 1983. Growth curves, dental emergence norms,and supplementary morphological observations in known-agecaptive orangutans. Am J Primatol 5:285–301.

Fossey D. 1979. Development in the mountain gorilla (Gorillagorilla beringei). In: Clutton-Brock TH, editor. Primate ecology:studies of feeding and ranging behaviour in lemurs, monkeys,and apes. London: Academic Press. p 415–447.

Fox GJ. 1984. Food transfer in gibbons. In: Preuschoft H, ChiversDJ, Brockelman WY, Creel N, editors. The lesser apes: evolu-tionary and behavioural biology. Edinburgh: Edinburgh Uni-versity Press. p 324–332.

Fragaszy D, Adams-Curtis L. 1997. Developmental changes inmanipulation in tufted capuchins (Cebus apella) from birththrough 2 years and their relation to foraging and weaning.J Comp Psychol 111:201–211.

Fragaszy DM, Bard K. 1997. Comparison and development andlife history in Pan and Cebus. Int J Primatol 18:683–701.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 205

Freed BZ. 1999. An introduction to the ecology of daylight-activelemurs. In: Dolhinow P, Fuentes A, editors. The nonhumanprimates. Mountain View, CA: Mayfield Publishing Co. p 123–132.

Froehlich JW, Thorington RW Jr, Otis JS. 1981. The demographyof howler monkeys (Alouatta palliata) on Barro ColoradoIsland, Panama. Int J Primatol 2:207–236.

Galdikas BMF. 1985. Subadult male orangutan sociality andreproductive behavior at Tanjung Putang. Am J Primatol 8:87–99.

Galliari CA. 1985. Dental eruption in captive-born Cebus apella:from birth to 30 months old. Primates 26:506–510.

Galliari CA, Colillas OJ. 1985. Sequences and timing of dentaleruption in Bolivian captive-born squirrel monkeys (Saimirisciureus). Am J Primatol 8:195–204.

Garbutt N. 1999. Mammals of Madagascar. New Haven: YaleUniversity Press.

Garland T Jr, Harvey PH, Ives AR. 1992. Procedures for theanalysis of comparative data using phylogenetically indepen-dent contrasts. Syst Biol 41:18–32.

Garland T Jr, Midford PE, Ives AR. 1999. An introduction tophylogenetically based statistical methods, with a new methodfor confidence intervals on ancestral values. Am Zool 39:374–388.

Geissmann T. 1991. Age of maturation of siamangs. Am J Prima-tol 23:11–22.

Gest TR, Siegel MI. 1983. The relationship between organweights and body weights, facial dimensions, and dental di-mensions in a population of olive baboons (Papio cynocephalusanubis). Am J Phys Anthropol 61:189–196.

Gibson D, Chu E. 1992. Management and behaviour of Francois’langur Presbytis francoisi francoisi at the Zoological Society ofSan Diego. Int Zoo Yrbk 31:184–191.

Gibson KR. 1986. Cognition, brain size and the extraction ofembedded food resources. In: Else J, Lee PC, editors. Primateontogeny, cogntion and social behavior. Cambridge: CambridgeUniversity Press. p 93–104.

Glander KE. 1980. Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53:25–36.

Glander KE, Fedigan LM, Fedigan L, Chapman C. 1991. Fieldmethods for capture and measurement of three monkey speciesin Costa Rica. Folia Primatol (Basel) 57:70–82.

Glander KE, Wright PC, Daniels PS, Merenlender AM. 1992.Morphometrics and testicle size of rain forest lemur speciesfrom southeastern Madagascar. J Hum Evol 22:1–17.

Godfrey LR, Petto AJ, Sutherland MR. In press, a. Dental ontog-eny and primate life histories: the case of the giant extinctindroids of Madagascar. In: Plavcan JM, Kay RF, van SchaikCP, Jungers WL, editors. Reconstructing behavior in the pri-mate fossil record. New York: Kluwer Academic/Plenum Press.

Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. In press,b. Dental development and primate life histories. In: KappelerPM, Pereira ME, editors. Primate life histories and socioecol-ogy. Chicago: University of Chicago Press.

Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior.Cambridge, MA: Harvard University Press.

Goo GP, Fugate JK. 1984. Effects of weaning age on maternalreproduction and offspring health in rhesus monkeys (Macacamulatta). Lab Anim Sci 34:66–69.

Goss AN. 1984. A comparison of tooth eruption patterns betweentwo colonies of young marmosets (Callithrix jacchus). J DentRes 63:44–46.

Gould L, Sussman RW, Sauther ML. 1999. Natural disasters andprimate populations: the effects of a 2-year drought on a natu-rally occurring population of ring-tailed lemurs (Lemur catta)in southwestern Madagascar. Int J Primatol 20:69–84.

Graham CE, Bown JA, Billhymer B, Cummins LB. 1985. Fetalmaturity estimation by lecithin/sphingomyelin ratios, preg-nancy duration, and caesarian section in chimpanzees. In: Gra-ham CE, Bowen JA, editors. Clinical managment of infantgreat apes. New York: Alan R. Liss. p 35–42.

Haddidian J, Bernstein IS. 1979. Female reproductive cycles andbirth data from an Old World monkey colony. Primates 20:429–442.

Hall RD, Beattie RJ, Wyckoff GH Jr. 1979. Weight gains andsequence of dental eruptions in infant owl monkeys (Aotustrivirgatus). In: Ruppenthal GC, editor. Nursery care of non-human primates. New York: Plenum Press. p 321–328.

Harcourt AH, Stewart KJ, Fossey D. 1981. Gorilla reproductionin the wild. In: Graham CE, editor. Reproductive biology of thegreat apes. New York: Academic Press. p 265–279.

Harcourt CS, Bearder SK. 1989. Comparison of Galago moholi insouthern Africa with Galago zanzibaricus in Kenya. Int J Pri-matol 10:35–45.

Hardin CJ, Liebherr G, Fairchild O. 1975. Artificial inseminationin chimpanzees Pan troglodytes. Int Zoo Yrbk 15:132–134.

Hartwig WC. 1996. Perinatal life history traits in New Worldmonkeys. Am J Primatol 40:99–130.

Harvey PH, Pagel MD. 1991. The comparative method in evolu-tionary biology. Oxford: University of Oxford Press.

Harvey PH, Purvis A. 1991. Comparative methods for explainingadaptations. Nature 351:619–624.

Harvey PH, Martin RD, Clutton-Brock TH. 1987. Life histories incomparative perspective. In: Smuts BB, Cheney DL, SeyfarthRM, Wrangham RW, Struhsaker TT, editors. Primate societies.Chicago: University of Chicago Press. p 181–196.

Hearn JP. 1982. The reproductive physiology of the commonmarmoset Callithrix jacchus in captivity. Int Zoo Yrbk 22:138–143.

Hemingway CA. 1996. Morphology and phenology of seeds andwhole fruit eaten by Milne-Edwards’ sifaka, Propithecus dia-dema edwardsi, in Ranomafana National Park, Madagascar.Int J Primatol 17:637–659.

Hemingway CA. 1998. Selectivity and variability in the diet ofMilne-Edwards’ sifakas (Propithecus diadema edwardsi). Im-plications for folivory and seed-eating. Int J Primatol 19:355–377.

Hernandez-Camacho J, Defler TR. 1985. Some aspects of theconservation of non-human primates in Colombia. PrimateConserv 6:42–50.

Hershkovitz P. 1977. Living New World monkeys (Platyrrhini),volume 1. Chicago: University of Chicago Press.

Hill WCO. 1934. A monograph on the purple-faced leaf-monkeys(Pithecus vetulus). Ceylon J Sci [B] 19:23–88.

Hill WCO. 1937. On the breeding and rearing of certain species ofprimates in captivity. Ceylon J Sci [B] 20:369–389.

Hladik CM. 1977. A comparative study of the feeding strategies oftwo sympatric species of leaf monkey: Presbytis senex and Pres-bytis entellus. In: Clutton-Brock TH, editor. Primate ecology:studies of feeding and ranging behaviour in lemurs, monkeys,and apes. New York: Academic Press. p 324–354.

Hollihn U. 1973. Remarks on the breeding and maintenance ofcolobus monkeys Colobus guereza, proboscis monkeys Nasalislarvatus and Douc langurs Pygathrix nemaeus in zoos. Int ZooYrbk 13:185–188.

Horwich R. 1974. Development of behaviors in a male spectacledlangur. Primates 15:151–178.

Horwich R, Manski D. 1975. Maternal care and infant transfer intwo species of colobus monkeys. Primates 16:49–73.

Hrdlicka A. 1925. Weight of the brain and of the internal organsin American monkeys. Am J Phys Anthropol 8:210–211.

Hrdy SB. 1980. The langurs of Abu: female and male strategies ofreproduction. Cambridge, MA: Harvard University Press.

Hurme VO, van Wagenen G. 1953. Basic data on the emergenceof deciduous teeth in the monkey (Macaca mulatta). Proc AmPhilos Soc 105:105–140.

Ibscher L. 1967. Geburt und fruhe Entwicklung zweier Gibbons(Hylobates lar l.). Folia Primatol (Basel) 5:43–69.

Iwamoto M, Hamada Y, Watanabe T. 1984. Eruption of perma-nent teeth in Japanese monkeys (Macaca fuscata). J AnthropolSoc Nippon 92:273–279.

Izard MK, Nash L. 1988. Contrasting reproductive parameters inGalago senegalensis braccatus and G. s. moholi. Int J Primatol9:519–527.

206 L.R. GODFREY ET AL.

Janson C, van Schaik C. 1993. Ecological risk aversion in juvenileprimates: slow and steady wins the race. In: Pereira ME, Fair-banks LA, editors. Juvenile primates: life history, developmentand behavior. New York: Oxford University Press. p 57–76.

Jay PC. 1965. The common langur of north India. In: DeVore I,editor. Primate behaviour: field studies of monkeys and apes.New York: Holt, Rinehart, and Winston. p 197–247.

Joffe TH. 1997. Social pressures have selected for an extendedjuvenile period in primates. J Hum Evol 32:593–605.

Johnston GW, Dreizen S, Levy BM. 1970. Dental development inthe cotton ear marmoset (Callithrix jacchus). Am J Phys An-thropol 33:41–48.

Jungers WL. 1988. New estimates of body size in australo-pithecines. In: Grine FE, editor. Evolutionary history of the“robust” australopithecines. New York: Aldine de Gruyer. p115–125.

Jungers WL. 1997. Orang-utans of the Menage Scientific Expe-dition to Borneo. Am J Phys Anthropol [Suppl] 24:138–139.

Jungers WL, Susman RL. 1984. Body size and skeleton allometryin African apes. In: Susman RL, editor. The pygmy chimpan-zee. New York: Plenum Press. p 131–177.

Jungers WL, Godfrey LR, Simons EL, Wunderlich RE, RichmondBG, Chatrath PS, Rakotosaminanana B. In press. Ecomorphol-ogy and behavior of giant extinct lemurs from Madagascar. In:Plavcan JM, Kay RF, van Schaik CP, Jungers WL, editors.Reconstructing behavior in the primate fossil record. NewYork: Kluwer Academic/Plenum Press.

Kappeler PM, Ganzhorn JU. 1993. The evolution of primate com-munities and societies in Madagascar. Evol Anthropol 2:159–171.

Kay RF. 1978. Molar structure and diet in extant Cercopitheci-dae. In: Butler PM, Joysey KA, editors. Development, functionand evolution of teeth. London: Academic Press. p 309–339.

Keiter MD. 1981. Hand-rearing and development of a lowlandgorilla at Woodland Park Zoo, Seattle. Int Zoo Yrbk 21:229–235.

Kelley J. 1999. Age at first molar emergence in Afropithecusturkanensis. Am J Phys Anthropol [Suppl] 28:167.

Kinzey WG. 1997. Synopsis of New World primates (16 genera).In: Kinzey WG, editor. New World primates: ecology, evolution,and behavior. New York: Aldine de Gruyter. p 167–324.

Kirkpatrick RC. 1999. Colobine diet and social organization. In:Dolhinow P, Fuentes A, editors. The nonhuman primates.Mountain View, CA: Mayfield Publishing Co. p 93–108.

Kirkwood JK, Stathatos K. 1992. Biology, rearing, and care ofyoung primates. Oxford: Oxford University Press.

Klopfer PH, Boskoff KJ. 1979. Maternal behavior in prosimians.In: Doyle GA, Martin RD, editors. The study of prosimianbehavior. New York: Academic Press. p 123–156.

Kozlowski J, Weiner J. 1997. Interspecific allometries are by-products of body size optimization. Am Nat 149:352–380.

Kushner H, Kraft-Schveyer N, Angelakos ET, Wudarski EM.1982. Analysis of reproductive data in a breeding colony ofAfrican green monkeys. J Med Primatol 11:77–84.

Kuster J. 1983. Longitudinal study of the physical development ofhand-reared common marmosets (Callithrix jacchus). In: SethPK, editor. Perspectives in primate biology. New Delhi: Today& Tomorrow. p 147–159.

Kuykendall KL, Mahoney CJ, Conroy GC. 1992. Probit and sur-vival analysis of tooth emergence ages in a mixed-longitudinalsample of chimpanzees (Pan troglodytes). Am J Phys Anthropol89:379–399.

Lee PC. 1996. The meanings of weaning: Growth, lactation, andlife history. Evol Anthropol 5:87–96.

Lee PC. 1999. Comparative ecology of postnatal growth andweaning among haplorhine primates. In: Lee PC, editor. Com-parative primate socioecology. Cambridge: Cambridge Univer-sity Press. p 111–139.

Lee PC, Majluf P, Gordon IJ. 1991. Growth, weaning and mater-nal investment from a comparative perspective. J Zool Lond225:99–114.

Leigh SR. 1994. Ontogenetic correlates of diet in anthropoidprimates. Am J Phys Anthropol 94:499–522.

Leskes A, Acheson NH. 1971. Social organization of a free-rang-ing troop of black and white colobus monkeys (Colobus abyssi-nicus). Proc Int Congr Primatol 3:22–31.

Lindburg DG. 1977. Feeding behavior and diet of rhesus ma-caques (Macaca mulatta) in a Siwalik forest in north India. In:Clutton-Brock TH, editor. Primate ecology: studies of feedingand ranging behaviour in lemurs, monkeys, and apes. NewYork: Academic Press. p 223–249.

MacArthur RH, Wilson EO. 1967. The theory of island biogeog-raphy. Princeton: Princeton University Press.

Malinow MR, Pope BL, Depaoli JR, Katz S. 1968. Laboratoryobservations on living howlers. Bibl Primatol 7:224–230.

Markham R. 1994. Doing it naturally: reproduction in captiveorangutans (Pongo pygmaeus). In: Ogden JJ, Perkins LA, Shee-ran L, editors. The neglected ape. San Diego: Zoological Societyof San Diego. p 166–170.

Markham R, Groves CP. 1990. Brief communication: weights ofwild orang utans. Am J Phys Anthropol 81:1–3.

Martin RD. 1983. Human brain evolution in an ecological context.New York: American Museum of Natural History.

Martin RD. 1990. Primate origins and evolution—a phylogeneticreconstruction. Princeton: Princeton University Press.

Martin RD. 1996. Scaling of the mammalian brain: the maternalenergy hypothesis. News Physiol Sci 11:149–156.

McKenna JJ. 1982. The evolution of primate societies, reproduc-tion and parenting. In: Fobes JL, King JE, editors. Primatebehaviour. London: Academic Press. p 87–133.

Medway L. 1970. Breeding of silvered leaf monkey, Presbytiscristata, in Malaya. J Mammal 51:630–632.

Melnick DJ, Pearl MC. 1987. Cercopithecines in multimalegroups: genetic diversity and population structure. In: SmutsBB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT,editors. Primate societies. Chicago: University of ChicagoPress. p 121–134.

Meyers DM. 1993. The effects of resource seasonality on behaviorand reproduction in the golden-crowned sifaka (Propithecustattersalli, Simons, 1988) in three Malagasy forests. Ph.D. dis-sertation, Duke University, Durham, North Carolina.

Meyers DM, Wright PC. 1993. Resource tracking: Food availabil-ity and Propithecus seasonal reproduction. In: Kappeler PM,Ganzhorn JU, editors. Lemur social systems and their ecolog-ical basis. New York: Plenum. p 179–192.

Middleton CC, Rosal J. 1972. Weights and measurements ofnormal squirrel monkeys (Saimiri sciureus). Lab Anim Sci22:583–586.

Miles P. 1967. Notes on the rearing and development of a hand-reared spider monkey Ateles geoffroyi. Int Zoo Yrbk 7:82–85.

Miller JMA. 1997. A hierarchical analysis of primate brain sizeand body size: patterns of morphometric variation. Ph.D. dis-sertation, University of Southern California, Los Angeles, Cal-ifornia.

Milton K. 1981. Estimates of reproductive parameters for free-ranging Ateles geoffroyi. Primates 22:574–579.

Mittermeier RA, Tattersall I, Konstant B, Meyers DM, Mast RB,editors. 1994. Lemurs of Madagascar. Washington, DC: Con-servation International.

Morbeck ME. 1997. Reading life history in teeth, bones, andfossils. In: Morbeck ME, Galloway A, Zihlman A, editors. Theevolving female. Princeton: Princeton University Press. p 117–131.

Napier PH. 1981. Catalogue of primates in the British Museum(Natural History) and elsewhere in the British Isles. Part II.Family Cercopithecidae, subfamily Cercopithecinae. London:British Museum (Natural History).

Napier PH. 1985. Catalogue of primates in the British Museum(Natural History) and elsewhere in the British Isles. Part III.Family Cercopithecidae, subfamily Colobinae. London: BritishMuseum (Natural History).

Nash L. 1993. Juveniles in nongregarious primates. In: PereiraME, Fairbanks LA, editors. Juvenile primates: life history,development and behavior. New York: Oxford University Press.p 119–137.

Neville MK, Glander KE, Braza F, Rylands AB. 1988. The howl-ing monkeys, genus Alouatta. In: Mittermeier RA, Rylands AB,

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 207

Coimbra-Filho AF, Fonseca GAB, editors. Ecology and behaviorof neotropical primates, volume 2. Washington, DC: WorldWildlife Fund. p 349–453.

Nishida T, Takasaki H, Takahata Y. 1990. Demography andreproductive profiles. In: Nishida T, editor. The chimpanzees ofthe Mahale mountains: sexual and life history strategies. To-kyo: University of Tokyo Press. p 63–98.

Oates JF, Davies AG, Delson E. 1994. The diversity of livingcolobines. In: Davies AG, Oates JF, editors. Colobine monkeys:their ecology, behavior, and evolution. Cambridge: CambridgeUniversity Press. p 45–73.

Ockerse T. 1959. The eruption sequence and eruption times of theteeth of the vervet monkey. J Dent Assoc S Afr 14:422–424.

Orgeldinger M. 1994. Monitoring body weight in captive pri-mates, with special reference to siamangs. Int Zoo News 41:17–26.

Overdorff DJ. 1993. Similarities, differences, and seasonal pat-terns in the diets of E. rubriventer and E. fulvus rufus inRanomafana National Park, Madagascar. Int J Primatol 14:721–752.

Overdorff DJ, Strait SG. 1998. Seed handling by three prosimianprimates in southeastern Madagacar: implications for seed dis-persal. Am J Primatol 45:69–82.

Overdorff DJ, Merenlender AM, Talata P, Telo A, Forward ZA.1999. Life history of Eulemur fulvus rufus from 1988–1992 insoutheastern Madagascar. Am J Phys Anthropol 108:295–310.

Pagel M. 1992. A method for the analysis of comparative data. JTheor Biol 156:431–432.

Patino E, Borda JT, Ruiz JC. 1996. Sexual maturity and seasonalreproduction in captive Cebus apella. Lab Primate Newslett35:8–10.

Payne J, Francis CM. 1985. A field guide to mammals of Borneo.Sabah, Malaysia: Sabah Society.

Pereira ME. 1993. Seasonal adjustment of growth rate and adultbody weight in ringtailed lemurs. In: Kappeler PM, GanzhornJU, editors. Lemur social systems and their ecological basis.New York: Plenum Press. p 205–221.

Peres CA. 1994. Which are the largest New World monkeys? JHum Evol 26:245–249.

Peters RH. 1983. The ecological implications of body size. Cam-bridge: Cambridge University Press.

Petter J-J, Albignac R, Rumpler Y. 1977. Faune de Madagascar:mammiferes lemuriens (Primates prosimiens). Paris: ORSTOM(CNRS).

Petter-Rousseaux A. 1962. Recherches sur la biologie de la repro-duction des primates inferieurs. Mammalia [Suppl] 26:1–88.

Pianka ER. 1970. On r- and K-selection. Am Nat 104:592–597.Pilbeam D. 1988. Primates. In: Harrison GA, Tanner JM, Pil-

beam D, Baker PT, editors. Human biology: an introduction tohuman evolution, variation, growth, and adaptability, 3rd ed.Oxford: Oxford University Press. p 27–71.

Pournelle GH. 1967. Observations on reproductive behaviour andearly postnatal development of the proboscis monkey (Nasalislarvatus orientalis). Int Zoo Yrbk 7:90–92.

Powzyk JA. 1996. A comparison of feeding strategies between thesympatric Indri indri and Propithecus diadema diadema inprimary rain forest. Am J Phys Anthropol [Suppl] 22:190.

Promislow DEL, Harvey PH. 1990. Living fast and dying young:a comparative analysis of life-history variation among mam-mals. J Zool Lond 220:417–437.

Purvis A, Harvey PH. 1995. Mammal life history evolution: acomparative test of Charnov’s model. J Zool Lond 237:259–283.

Pusey A. 1990. Behavioral changes at adolescence in chimpan-zees. Behaviour 115:203–246.

Rasamimanana HR, Rafidinarivo E. 1993. Feeding behavior ofLemur catta females in relation to their physiological state. In:Kappeler PM, Ganzhorn JU, editors. Lemur social systems andtheir ecological basis. NewYork: Plenum Press. p 123–133.

Ravosa MJ, Meyers DM, Glander KE. 1993. Relative growth ofthe limbs and trunk in sifakas: heterochronic, ecological, andfunctional considerations. Am J Phys Anthropol 92:499–520.

Reed DJ, Schwartz GT, Dean C, Chandrasekera MS. 1998. Ahistological reconstruction of dental development in the com-mon chimpanzee, Pan troglodytes. J Hum Evol 35:427–448.

Richard AF, Rakotomanga P, Schwartz M. 1993. Dispersal byPropithecus verreauxi at Beza Mahafaly, Madagascar: 1984–1991. Am J Primatol 30:1–20.

Roberts M. 1994. Growth, development, and parental care in thewestern tarsier (Tarsius bancanus) in captivity: evidence for a“slow” life-history and nonmonogamous mating system. Int JPrimatol 15:1–28.

Robinson JG, Janson CH. 1987. Capuchins, squirrel monkeys,and atelines: socioecological convergence with Old World Pri-mates. In: Smuts BB, Cheney DL, Seyfarth RM, WranghamRW, Struhsaker TT, editors. Primate societies. Chicago: Uni-versity of Chicago Press. p 69–82.

Ross C. 1991. Life history patterns of New World monkeys. Int JPrimatol 12:481–502.

Ross C. 1992. Basal metabolic rate, body weight, and diet inprimates: an evaluation of the evidence. Folia Primatol (Basel)58:7–23.

Ross C, Jones KE. 1999. Socioecology and the evolution of primatereproductive rates. In: Lee PC, editor. Comparative primatesocioecology. Cambridge: Cambridge University Press. p 73–110.

Rudran R. 1973. The reproductive cycles of two subspecies ofpurple-faced langurs (Presbytis senex) with relation to environ-mental factors. Folia Primatol (Basel) 19:41–60.

Ruedi D. 1981. Hand-rearing and reintegration of a caesarian-born proboscis monkey Nasalis larvatus at Basle Zoo. Int ZooYrbk 21:225–229.

Rumbaugh DM. 1965. The gibbon infant, Gabrielle: its growthand development. Zoonooz 38:10–15.

Rumbaugh DM. 1967. The siamang infant, Sarah: its growth anddevelopment. Zoonooz 40:12–18.

Rumiz DI. 1990. Alouatta caraya: population density and demog-raphy in northern Argentina. Am J Primatol 21:279–294.

Sauther ML. 1991. Reproductive behavior of free-ranging Lemurcatta at Beza Mahafaly Special Reserve, Madagascar. Am JPhys Anthropol 84:463–477.

Schmid J, Ganzhorn JU. 1996. Resting metabolic rates of Lepile-mur ruficaudatus. Am J Primatol 38:169–174.

Schultz AH. 1941. The relative size of the cranial capacity inprimates. Am J Phys Anthropol 28:273–287.

Schultz AH. 1942. Growth and development of the proboscismonkey. Bull Mus Comp Zool Harvard 89:279–314.

Schwartz SM, Kemnitz JW. 1992. Age- and gender-relatedchanges in body size, adiposity, and endocrine and metabolicparameters in free ranging rhesus macaques. Am J Phys An-thropol 89:109–121.

Siegel MI, Sciulli PW. 1973. Eruption sequences of the deciduousdentition of Papio cynocephalus. J Med Primatol 2:247–248.

Sirianni JE, Swindler DR. 1985. Growth and development of thepigtailed macaque. Boca Raton, FL: CRC Press.

Skinner JD, Smithers RHN. 1990. The mammals of the southernAfrican subregion. Pretoria, South Africa: University of Preto-ria.

Smith BH. 1989. Dental development as a measure of life historyin primates. Evolution 4:683–688.

Smith BH. 1992. Life history and the evolution of human matu-ration. Evol Anthropol 1:134–142.

Smith BH, Crummett TL, Brandt KL. 1994. Ages of eruption ofprimate teeth: a compendium for aging individuals and com-paring life histories. Yrbk Phys Anthropol 37:177–231.

Smith GE. 1908. On the form of the brain in the extinct lemurs ofMadagascar, with some remarks on the the affinities of theIndrisinae. Trans Zool Soc Lond 18:163–177.

Smith RJ. 1994. Degrees of freedom in interspecific allometry: anadjustment for the effects of phylogenetic constraint. Am JPhys Anthropol 93:95–107.

Smith RJ. 1999. Statistics of sexual size dimorphism. J Hum Evol36:423–459.

Smith RJ, Jungers WL. 1997. Body mass in comparative prima-tology. J Hum Evol 32:523–559.

Smith RJ, Gannon PJ, Smith BH. 1995. Ontogeny of australo-pithecines and early Homo: evidence from cranial capacity anddental eruption. J Hum Evol 29:155–168.

208 L.R. GODFREY ET AL.

Snowdon CT, Soini P. 1988. The tamarins, genus Saguinus. In:Mittermeier RA, Rylands AB, Coimbra-Filho AF, da FonescaGAB, editors. Ecology and behavior of neotropical primates,volume 2. Washington, DC: World Wildlife Fund. p 223–298.

Sodaro V. 1993. Hand-rearing and reintroduction of a black-handed spider monkey Ateles geoffroyi at Brookfield Zoo, Chi-cago. Int Zoo Yrbk 32:224–228.

Sommer V, Srivastava A, Borries C. 1992. Cycles, sexuality, andconception in free-ranging langurs (Presbytis entellus). Am JPrimatol 28:9–27.

Stearns SC. 1992. The evolution of life histories. Oxford: OxfordUniversity Press.

Stephan H, Frahm H, Baron G. 1981. New and revised data onvolumes of brain structures in insectivores and primates. FoliaPrimatol (Basel) 35:1–29.

Strier KB. 1999. The atelines. In: Dolhinow P, Fuentes A, editors.The nonhuman primates. Mountain View, CA: Mayfield Pub-lishing Co. p 109–114.

Struhsaker TT. 1975. The red colobus monkey. Chicago: Univer-sity of Chicago Press.

Struhsaker TT, Leland L. 1987. Colobines: infanticide by adultmales. In: Smuts BB, Cheney DL, Seyfarth RM, WranghamRW, Struhsaker TT, editors. Primate societies. Chicago: Uni-versity of Chicago Press. p 83–97.

Sugiyama Y. 1965. Behavioral development and social structurein two troops of Hanuman langurs (Presbytis entellus). Pri-mates 6:381–418.

Sussman RW. 1974. Ecological distinctions in sympatric speciesof Lemur. In: Martin RD, Doyle GA, Walker AC, editors. Pro-simian biology. London: Duckworth. p 75–108.

Sussman RW. 1991. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagas-car. Am J Phys Anthropol 84:43–58.

Sussman RW. 1992. Male life history and intergroup mobilityamong ringtailed lemurs (Lemur catta). Int J Primatol 13:395–414.

Swindler DR. 1976. Dentition of living primates. London: Aca-demic Press.

Tan C. 1999a. Group composition, home range size and diet ofthree sympatric bamboo lemur species (genus Hapalemur) inRanomafana National Park, Madagascar. Int J Primatol 20:547–566.

Tan C. 1999b. Life history and infant rearing strategies of threeHapalemur species. Primate Rep 54:33.

Taylor SCS. 1965. A relation between mature weight and timetaken to mature in mammals. Anim Product 7:203–220.

Terranova CJ, Coffman BS. 1997. Body weights of wild andcaptive lemurs. Zoo Biol 16:17–30.

Thorington RW Jr, Rudran R, Mack D. 1979. Sexual dimorphismof Alouatta seniculus and observations on capture techniques.In: Eisenberg JG, editor. Vertebrate ecology in the northernneotropics. Washington, DC: Smithsonian Institution Press. p97–106.

Tobias PV. 1994. The craniocerebral interface in early hominids.In: Corruccini RS, Ciochon RL, editors. Integrative paths to thepast: paleoanthropological advances in honor of F. Clark How-ell. Englewood Cliffs, NJ: Prentice Hall. p 185–203.

Treves A. 1996. A preliminary analysis of the timing of infantexploration in relation to social structure in 17 primate species.Folia Primatol (Basel) 67:152–156.

Turner TR, Anapol F, Jolly CJ. 1994. Body weights of adult vervetmonkeys (Cercopithecus aethiops) at four sites in Kenya. FoliaPrimatol (Basel) 63:177–179.

Tutin C. 1994. Reproductive success story: variability amongchimpanzees and comparison with gorillas. In: Wrangham RW,McGrew WC, de Waal F, Heltne P, editors. Chimpanzee cul-tures. Cambridge, MA: Harvard University Press. p 181–193.

Uehara S, Nishida T. 1987. Body weights of wild chimpanzees(Pan troglodytes schweinfurthii) of the Mahale Mountains Na-tional Park, Tanzania. Am J Phys Anthropol 72:315–321.

Van Horn RN, Eaton GG. 1979. Reproductive physiology andbehavior in prosimians. In: Doyle GA, Martin RD, editors. Thestudy of prosimian behavior. New York: Academic Press. p.79–122.

van Roosmalen MGM. 1985. Habitat preferences, diet, feedingstrategy, and social organization of the black spider monkey(Ateles paniscus) in Surinam. Acta Amazon [Suppl] 15:1–238.

Watts DP. 1991. Mountain gorilla reproduction and sexual be-havior. Am J Primatol 24:211–226.

Watts DP, Pusey A. 1993. Behavior of juvenile and adolescentgreat apes. In: Pereira ME, Fairbanks LA, editors. Juvenileprimates: life history, development, and behavior. New York:Oxford University Press. p 148–172.

Western D. 1979. Size, life history and ecology in mammals. AfrJ Ecol 17:185–204.

Wilen R, Naftolin F. 1978. Pubertal age, weight, and weight gainin the individual female New World Monkey (Cebus albifrons).Primates 19:769–794.

Willis MS. 1995. Dental variation in Asian colobines. Ph.D. dis-sertation, Washington University.

Willoughby DP. 1978. All about gorillas. South Brunswick, NJ:A.S. Barnes & Noble.

Winkler P, Loch H, Vogel C. 1984. Life history of hanumanlangurs (Presbytis entellus). Folia Primatol (Basel) 43:1–23.

Winter M 1978. Investigation of the sequence of tooth eruption inhand-reared Callithrix jacchus. In: Rothe H, Wolters H-J,Hearn JP, editors. Biology and behavior of marmosets. Pro-ceedings of the Marmoset Workshop, Gottingen, September1977. Gottingen: Eigenverlag Rothe. p 109–124.

Wolfe LG. 1986. Reproductive biology of rhesus and Japanesemacaques. Primates 27:95–101.

Wooldridge FL. 1971. Colobus guereza: birth and infant develop-ment in captivity. Animal Behaviour 19:481–485.

Wright PC. 1984. Biparental care in Aotus trivirgatus and Calli-cebus moloch. In: Small MF, editor. Female primates: studiesby women primatologists. New York: Liss. p 59–75.

Wright PC. 1990. Patterns of parental care in primates. Int JPrimatol 11:89–102.

Wright PC. 1995. Demography and life history of free-rangingPropithecus diadema edwardsi in Ranomafana National Park,Madagascar. Int J Primatol 16:835–854.

Wright PC. 1997. Behavioral and ecological comparisons of Neo-tropical and Malagasy primates. In: Kinzey WG, editor. NewWorld primates: ecology, evolution, and behavior. New York:Aldine de Gruyter. p 127–141.

Wright PC. 1999. Lemur traits and Madagascar ecology: copingwith an island environment. Yrbk Phys Anthropol 42:31–72.

Yamashita N. 1998a. Molar morphology and variation in twoMalagasy lemur families (Lemuridae and Indriidae). J HumEvol 35:137–162.

Yamashita N. 1998b. Functional dental correlates of food prop-erties in five Malagasy lemur species. Am J Phys Anthropol106:169–188.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 209

APPENDIX A. Life history data, including postcanine dentition at selected ages and life cycle stages(teeth in parentheses may be erupting)

TaxonAdult mass,

(kg)

Adult /cranial

capacity (cc)

Postcaninedentition at

4 months

Postcaninedentition at

1 year

Age atweaning,in years

Postcaninedentition at

weaning

Age at / firstbreeding, in

years

Propithecustattersalli

3.39 ? 30.5 dp2 dp33 dp4

4 P3 P2 P44 M1

1 0.42 dp2 dp3 P44 M1

1 4.53.5 / M1

1 (M22) M2

2 M33 M2

2

Propithecusverreauxi

3.48 ? 29.7 dp2 dp33 dp4

4 P3 P2 P44 M1

1 0.50 dp2 dp3 dp44 4.57

3.62 / M11 (M2

2) M22 M3

3 M11 M2

2 (P44)

Propithecus diadema 5.94 ? 40.0 dp2 dp33 dp4

4 P3 P2 P44 M1

1 0.50 dp2 dp3 dp44 4.51

6.26 / M11 M2

2 M33 M1

1 M22 (P4

4)Avahi laniger 0.92 ? 9.8 P3 P2 P4

4 P3 P2 P44 M1

1 0.41 P3 P2 P44 M1

1 2.581.05 / M2

1 M22 M2

2 M33 M2

2

Varecia variegata 3.63 ? 31.2 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.40 dp22 dp3

3 dp44 2.72

3.52 / M11 M2

2

Hapalemur griseus 0.748 ? 14.6 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.33 dp22 dp3

3 dp44 2.73

0.670 / M11 M2

2 (P44)

Lemur catta 2.21 ? 23.4 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.49 dp22 dp3

3 dp44 2.63

2.21 / (M1) M11 M2

2 (P4) M11

Eulemur macaco 2.37 ? 24.6 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.37 dp22 dp3

3 dp44 1.66

2.51 / M11 M2

2 (M1)Eulemur fulvus 2.18 ? 25.6 dp2

2 dp33 dp4

4 dp22 dp3

3 dp44 0.50 dp2

2 dp33 dp4

4 2.662.25 / M1

1 (M22) (M1

1)Lepilemur

ruficaudatus0.761 ? 7.4 dp2

2 dp33 dp4

4 P22 P3

3 P44 0.33 dp2

2 dp33 dp4

4 1.630.779 / M1

1 M22 (M3

3

P44)

M11 M2

2 M33 M1

1 M22 (M3

3 P44)

Galago moholi 0.187 ? 3.6 P22 dp3

3 P44 P2

2 P33 P4

4 0.23 dp22 dp3

3 dp44 0.71

0.173 / M11 M2

2 M33 M1

1 M22 M3

3 M11 M2

2 M33 (P2

2)Callithrix jacchus 0.362 ? 7.7 dp2

2 dp33 dp4

4 P22 P3

3 P44 0.21 dp2

2 dp33 dp4

4 1.670.381 / M1

1 M11 M2

2

Saguinus nigricollis 0.468 ? 8.9 dp22 dp3

3 dp44 P2

2 P33 P4

4 0.21 dp22 dp3

3 dp44 2.33

0.484 / M11 M1

1 M22

Saguinus fuscicollis 0.343 ? 8.2 dp22 dp3

3 dp44 P2

2 P33 P4

4 0.25 dp22 dp3

3 dp44 2.33

0.358 / M11 M2

2

Saimiri sciureus 0.779 ? 23.2 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.50 dp22 dp3

3 dp44 2.50

0.662 / M11 M2

2 M11

Cebus albifrons 3.18 ? 56.8 dp22 dp3

3 dp22 dp3

3 dp44 0.75 dp2

2 dp33 dp4

4 4.002.29 / (M1

1)Cebus apella 3.65 ? 63.1 dp2

2 dp33 dp2

2 dp33 dp4

4 1.14 dp22 dp3

3 dp44 5.78

2.52 / (M11)

Aotus trivirgatus 0.813 ? 16.1 dp22 dp3

3 dp44 dp2

2 P33 P4

4 0.49 dp22 dp3

3 dp44 2.42

0.736 / M11 M2

2 M33 M1

1

Alouatta palliata 7.16 ? 55.4 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.89 dp22 dp3

3 dp44 3.99

5.33 / M11 M1

1

Alouatta caraya 6.42 ? 47.9 dp22 dp3

3 dp44 dp2

2 dp33 dp4

4 0.89 dp22 dp3

3 dp44 3.71

4.33 / M11 M2

2 (M11)

Ateles geoffroyi 7.78 ? 106.4 dp22 dp3

3 dp22 dp3

3 dp44 2.25 dp2

2 dp33 dp4

4 6.397.29 / M1

1 M11 M2

2

Chlorocebus aethiops 4.26 ? 59.2 dp33 dp4

4 dp33 dp4

4 M11 0.60 dp3

3 dp44 4.75

2.98 /Macaca fascicularis 5.36 ? 62.5 dp3

3 dp33 dp4

4 1.17 dp33 dp4

4 3.903.59 /

Macaca mulatta 10.61 ? 81.3 dp33 dp3

3 dp44 0.88 dp3

3 dp44 4.19

7.97 /Macaca nemestrina 11.2 ? 96.2 dp3

3 dp33 dp4

4 1.00 dp33 dp4

4 3.906.5 /

Papio cynocephalus(excluding kindae)

24.9 ? 145.5 (dp3) dp33 dp4

4 1.25 dp33 dp4

4 5.5013.6 /

Papio anubis 25.1 ? 158.9 (dp3) dp33 dp4

4 1.6 dp33 dp4

4 4.5013.3 /

Kasi vetulus 8.2 ? 56.6 dp33 dp4

4 dp33 dp4

4 0.60 dp33 dp4

4 4.05.9 / (M1

1)Semnopithecus

entellus15.3 ? 98.2 dp3

3 dp33 dp4

4 1.14 dp33 dp4

4 3.9010.9 / (M1

1) (M11)

Trachypithecusfrancoisi

8.0 ? 66.9 dp33 dp4

4 dp33 dp4

4 M11 1.08 dp3

3 dp44 M1

1 4.07.3 / (M2

2) (M22)

Trachypithecuscristata

6.61 ? 54.5 dp33 dp4

4 dp33 dp4

4 M11 1.0 dp3

3 dp44 M1

1 4.05.76 /

Trachypithecusobscura

7.9 ? 60.8 dp33 dp3

3 dp44 1.00 dp3

3 dp44 4.0

6.26 / (M11) (M1

1)Nasalis larvatus 20.39 ? 82.8 dp3

3 dp44 dp3

3 dp44 M1

1 0.77 dp33 dp4

4 4.59.83 ?

(Continued)

210 L.R. GODFREY ET AL.

APPENDIX A

TaxonAdult mass,

(kg)

Adult /cranial

capacity (cc)

Postcaninedentition at

4 months

Postcaninedentition at

1 year

Age atweaning,in years

Postcaninedentition at

weaning

Age at / firstbreeding, in

years

Piliocolobus badius 12.3 ? 64.8 dp33 dp4

4 dp33 dp4

4 M11 1.43 dp3

3 dp44 M1

1 4.088.25 / M2

2 M22 (P3

3 P44)

Colobus guereza 13.5 ? 69.0 dp33 dp4

4 dp33 dp4

4 M11 1.08 dp3

3 dp44 M1

1 4.759.2 / (M2

2) (M22)

Hylobates lar 5.90 ? 102.2 dp33 dp3

3 dp44 1.50 dp3

3 dp44 6.69

5.34 /Hylobates

syndactylus11.9 ? 113.5 dp3

3 dp33 dp4

4 1.75 dp33 dp4

4 M11 5.18

10.7 /Pongo pygmaeus 78.2 ? 374.5 dp3

3 dp44 5.0 dp3

3 dp44 M1

1 14.3235.7 / M2

2

Pan troglodytes 49.6 ? 371.1 dp33 dp4

4 5.0 dp33 dp4

4 M11 13.90

40.4 /Gorilla gorilla 169.4 ? 455.6 dp3

3 dp44 3.5 dp3

3 dp44 M1

1 10.380.0 /

APPENDIX B. Sources for life history data, cranial capacities, and dental schedules, with notes

Genus and species Notes Sources

P. tattersalli Estimates uncertain due to small sample size.Sample includes one immature captivespecimen of known age. Dentition at 1 yearand age at first breeding estimated on basis ofgrowth records and comparisons with P.verreauxi and P. diadema. Cranial capacitybased on single adult male specimen atAmerican Museum of Natural History.

Meyers (1993), Meyers and Wright (1993), Ravosa et al.(1993), and growth records of Duke University PrimateCenter.

Propithecus verreauxi Dental eruption schedule reconstructed usingEaglen (1985), Smith et al. (1994), captivespecimens of known age, and immature wild-caught specimens aged on basis of collectiondate. Mean cranial capacity calculated forpooled sexes.

Eaglen (1984), Garbutt (1999), Martin (1990), Ravosa etal. (1993), Richard et al. (1993), Roberts (1994), Smithet al. (1994), Stephan et al. (1981), and records of DukeUniversity Primate Center.

Propithecus diadema Dental eruption schedule reconstructed usingcaptive and wild specimens of known age, andimmature wild-caught specimens aged onbasis of collection date. Adult body masscalculated for pooled subspecies.

Glander et al. (1992), Meyers and Wright (1993), Miller(1997), Powzyk (1996), Smith and Jungers (1997),Wright (1995), and personal communication from ClaireHemingway and Patricia Wright.

Avahi laniger Dental eruption schedule reconstructed usingimmature wild-caught specimens aged onbasis of collection date. Age at female firstbreeding estimated using estimates of age atfirst emigration from social group andgestation length, assuming reproductivesynchrony. Cranial capacity based on pooledsexes.

Albignac (1981), Glander et al. (1992), Martin (1990),Petter-Rousseaux (1962), and personal communicationfrom Patricia Wright.

Varecia variegata Dental eruption schedule reconstructed usingSmith et al. (1994), Eaglen (1985), captivespecimens of known age and immature wild-caught specimens aged on basis of collectiondate. Body mass values based on V. v.variegata.

Brockman et al. (1987), Cartmill et al. (1979), Eaglen(1985), Foerg (1982), Garbutt (1999), Miller (1997),Smith et al. (1994), Terranova and Coffman (1997), andrecords of Duke University Primate Center and ParcTsimbazaza.

Hapalemur griseus Dental eruption schedule reconstructed usingimmature wild-caught specimens aged onbasis of collection date.

Garbutt (1999), Tan (1999a,b), Wright (1990), andpersonal communication from Christina Grassi andChia Tan.

Lemur catta Dental eruption schedule reconstructed usingdata from Eaglen (1985), Smith et al. (1994),captive specimens of known age, andimmature wild-caught specimens aged onbasis of collection date.

Eaglen (1985), Gould et al. (1999), Hrdlicka (1925),Klopfer and Boskoff (1979), Mittermeier et al. (1994),Pereira (1993), Rasamimanana and Rafindinarivo(1993), Smith et al. (1994), Sussman (1991, 1992), andrecords of Duke University Primate Center and ZurichZoo.

Eulemur macaco Dental eruption schedule reconstructed usingSmith et al. (1994), Eaglen (1985), captivespecimens of known age, and immature wild-caught specimens aged on basis of collectiondate. Body mass based on means for the twosubspecies, captive individuals.

Colquhoun (1993), Eaglen (1985), Roberts (1994), Smith(1908), Smith et al. (1994), Smith and Jungers (1997),and records of Duke University Primate Center,Ivoloina and Oregon Regional Primate Center.

(Continued)

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 211

APPENDIX A (Continued)

Genus and species Notes Sources

Eulemur fulvus Dental eruption schedule reconstructed usingEaglen (1985), Smith et al. (1994), captivespecimens of known age, and immature wild-caught specimens aged on basis of collectiondate. Body mass values based on means for E.f. rufus. Adult female cranial capacity basedon Smith (1908) and unpublished data fromthe United States National Museum.

Eaglen (1985), Eisenberg (1981), Glander et al. (1992),Kappeler and Ganzhorn (1993), Overdorff et al. (1999),Roberts (1994), Smith (1908), Smith et al. (1994), andrecords of Ivoloina, Duke University Primate Center,and Indianapolis Zoo.

Lepilemurruficaudatus

Dental eruption schedule reconstructed usingimmature wild-caught specimens aged onbasis of collection date. Estimate for weaningbased on value reported for “L. mustelinus.”

Bauchot and Stephan (1966), Garbutt (1999), Nash(1993), Peter et al. (1977), Schmid and Ganzhorn(1996), Smith and Jungers (1997).

Galago moholi Dental eruption schedule reconstructed usingimmature wild-caught specimens aged onbasis of collection date or mass, and known-aged captive specimens, plus data in Smith etal. (1994) and comparisons to G. senegalensisgrowth records.

Doyle (1979), Harcourt and Bearder (1989), Izard andNash (1988), Kirkwood and Strathatos (1992), Nash(1993), Skinner and Smithers (1990), Smith et al.(1994), Van Horn and Eaton (1979).

Callithrix jacchus Dental eruption schedule from Smith et al.(1994), Swindler (1976), and Winter (1978).

Epple (1970), Goss (1984), Hearn (1982), Johnston et al.(1970), Kuster (1983), Miller (1997), Ross (1991), Smithet al. (1994), Swindler (1976), Winter (1978).

Saguinus nigricollis Dental eruption schedule from Chase andCooper (1969) and Smith et al. (1994). Age atfemale first breeding estimated on basis ofpublished values for closely related S.fuscicollis. Cranial capacity based on pooledsex data.

Chase and Cooper (1969), Harvey et al. (1987),Hernandez-Camacho and Defler (1985), Hershkovitz(1977), Ross and Jones (1999), Smith et al. (1994),Smith et al. (1995), Snowdon and Soini (1988).

S. fuscicollis Dental eruption schedule based on Smith etal. (1994) and Snowdon and Soini (1988).Cranial capacity based on pooled sex data.

Harvey et al. (1987), Ross and Jones (1999), Smith etal. (1994), Smith et al. (1995), Snowdon and Soini(1988).

Saimiri sciureus Data on dental eruption from Galliari andColillas (1985), Hershkovitz (1977), and Smithet al. (1994).

Baldwin and Baldwin (1981), Baldwin (1985), Galliariand Colillas (1985), Hershkovitz (1977), Kinzey (1997),Middleton and Rosal (1972), Miller (1997), Smith et al.(1994).

Cebus albifrons Data on dental eruption from Fleagle andSchaffler (1982).

Fleagle and Schaffler (1982), Hernandez-Camacho andDefler (1985), Miller (1997), Ross (1991), Smith andJungers (1997), Wilen and Naftolin (1978).

Cebus apella Data on dental eruption from Galliari (1985)and Smith et al. (1994)

Ayers (1986), Eisenberg (1989), Fleagle andMittermeier (1980), Fragaszy and Adams-Curtis (1997),Fragaszy and Bard (1997), Galliari (1985), Hernandez-Camacho and Defler (1985), Miller (1997), Patino et al.(1996), Robinson and Janson (1987), Ross (1991); Smithand Jungers (1997).

Aotus trivirgatus Data on dental eruption are from Hall et al.(1979). Data on weaning are taken fromrecords compiled at Woodland Park ZoologicalGardens.

Hall et al. (1979), Kinzey (1997), Miller (1997), Ross(1991), Smith and Jungers (1997), Wright (1984, 1997).

Alouatta palliata Dental eruption schedule inferred from datapresented by Froehlich et al. (1981), Glander(1980), and Neville et al. (1988).

Clarke (1990), Froehlich et al. (1981), Fedigan and Rose(1995), Glander (1980), Glander et al. (1991), Hartwig(1996), Kinzey (1997), Neville et al. (1988), Peres(1994), Smith and Jungers (1997), Thorington et al.(1979).

A. caraya Dental eruption schedule inferred from datapresented by Malinow et al. (1968) andNeville et al. (1988).

Malinow et al. (1968), Miller (1997), Neville et al.(1988), Ross and Jones (1999), Rumiz (1990), andrecords of Cheyenne Mountain Zoological Park andAudobon Park and Zoological Gardens.

Ateles geoffroyi Dental eruption schedule inferred on basis ofpublished comparisons with Cebus as well asa few records for Ateles geoffroyi (Carpenter,1935; Miles, 1967; Smith et al., 1994; Sodaro,1993). Dentition at weaning estimated onbasis of eruption schedule for Cebus coupledwith late age at weaning in Ateles.

Carpenter (1935), Chapman (1987), Eisenberg (1981),Fedigan and Rose (1995), Glander et al. (1991), Miles(1967), Miller (1997), Milton (1981), Robinson andJanson (1987), Schultz (1941), Smith et al. (1994),Sodaro (1993), Strier (1999), van Roosmalen (1985), andrecords of Pittsburgh Zoo.

Chlorocebus aethiops Dental eruption schedule from Smith et al.(1994) and Ockerse (1959)

Butynski (1988), Kushner et al. (1982), Melnick andPearl (1987), Miller (1997), Ockerse (1995), Ross (1991),Smith et al. (1994), Turner et al. (1994).

Macaca fascicularis Dental eruption schedule from Smith et al.(1994) and Iwamoto et al. (1984).

Fooden (1995), Harvey et al. (1987), Iwamoto et al.(1984), Miller (1997), Ross (1991), Smith et al. (1994).

(Continued)

212 L.R. GODFREY ET AL.

APPENDIX B (Continued)

Genus and species Notes Sources

M. mulatta Dental eruption schedule from Smith et al.(1994) and Hurme and van Wagenen (1953).

Goo and Fugate (1984) Haddidian and Bernstein(1979), Hurme and van Wagenen (1953), Lindburg(1977), Melnick and Pearl (1987), Miller (1997), Napier(1981), Ross (1991), Schwartz and Kemnitz (1992),Smith et al. (1994), Treves (1996).

M. nemestrina Dental eruption schedule from Smith et al.(1994) and Sirianni and Swindler (1985).

Fooden (1975), Harvey et al. (1987), Miller (1997), Ross(1991), Sirianni and Swindler (1985).

Papio cynocephalus Dental eruption schedule from Smith et al.(1994) and Siegel and Sciulli (1973).

Bentley-Condit and Smith (1997), Lee (1999), Miller(1997), Napier (1981), Ross (1991), Siegel and Sciulli(1973), Smith et al. (1994).

Papio anubis Dental eruption schedule from Smith et al.(1994).

Eley et al. (1989), Gest and Siegel (1983), Lee (1999),Miller (1997), Melnick and Pearl (1987), Popp (1983),Smith et al. (1994).

Kasi vetulus Dental schedule reconstructed using data onbody mass, coat color, Hill (1937), Leigh’s(1994) growth curves, and Smith et al. (1994).

Harvey et al. (1987), Hladik (1977), Hill (1934, 1937),Leigh (1994), Miller (1997), Napier (1985), Rudran(1973), Smith et al. (1994), Smith and Jungers (1997).

Semnopithecusentellus

Dental schedule reconstructed using data onbody mass, coat color (Sugiyama, 1965; Jay,1965; Winkler et al., 1984), Leigh’s (1994)growth curves, and known-aged captiveindividuals from collections of San DiegoState University and California PrimateResearch Center at Davis.

Hrdy (1980), Jay (1965), Leigh (1994), Miller (1997),Napier (1985), Sommer et al. (1992), Struhsaker andLeland (1987), Sugiyama (1965), Willis (1995), Winkleret al. (1984).

Trachypithecusfrancoisi

Dental schedule uncertain due to smallavailable sample of skulls. Known-agedindividuals housed at San Diego StateUniversity establish accelerated dentaleruption schedule. Cranial capacity estimatedusing regression analysis of adult / cranialvolume on adult / skull size for colobinesonly.

Gibson and Chu (1992), Willis (1995), and records ofSan Diego State University.

Trachypithecuscristata

Age at weaning and first breeding wereestimated on basis of review by Brandon-Jones (1985). Dental schedule reconstructedusing data on body mass, coat color(Bernstein, 1968; Payne and Francis, 1985),and Leigh’s (1994) growth curves.

Bernstein (1968), Brandon-Jones (1985), Leigh (1994),Medway (1970), Miller (1997), Payne and Francis(1985), Willis (1995), and personal communication fromJacqui Browman.

Trachypithecusobscura

Dental schedules were reconstructed usingdata on body mass, coat color, Leigh’s (1994)growth curves, one known-aged individualfrom Anthropological Institute and Museumin Zurich, and observations by Horwich(1974). Age at weaning and female firstbreeding estimated on basis of review byBrandon-Jones (1985).

Brandon-Jones (1985), Curtin and Chivers (1978),Horwich (1974), Leigh (1994), Miller (1997), Smith andJungers (1997).

Nasalis larvatus Dental schedule reconstructed using data onbody mass, coat color (Brandon-Jones, 1985;Payne and Francis, 1985), and Ruedi (1981)growth curves. On the basis of an observationby Schultz (1942) that actually pertains tomacaques, Napier (1985) incorrectly reportsfull eruption of the permanent dentition at 7years. Schultz (1942) actually states thatdental eruption in female proboscis monkeysis complete prior to sexual maturation.

Brandon-Jones (1985), Hollihn (1973), Kirkwood andStathatos (1992), Miller (1997), Payne and Francis(1985), Pournelle (1967), Ross (1992), Ruedi (1981),Schultz (1942), Smith and Jungers (1997).

Colobus guereza Dental schedule reconstructed using data onbody mass (Natural History Museum,London), coat color (Crandall, 1964; Horwichand Manski, 1975; Leskes and Acheson, 1971;Wooldridge, 1971), and Leigh’s (1994) growthcurves.

Crandall (1964), Harvey et al. (1987), Horwich andManski (1975), Leigh (1994), Leskes and Acheson(1971), Miller (1997), Oates et al. (1994), Ross andJones (1999), Smith and Jungers (1997), Wooldridge(1971), and records of Colombus Zoological Gardens.

Piliocolobus badius Dental schedule reconstructed using data onbody mass, coat color (Struhsaker, 1975), andLeigh’s (1994) growth curves. Body mass datafor P. b. oustaleti.

Leigh (1994), Miller (1997), Oates et al. (1994), Rossand Jones (1999), Smith and Jungers (1997),Struhsaker (1975).

Hylobates lar Dental eruption schedule from Ibscher (1967),Rumbaugh (1965, 1967), and Smith et al.(1994).

Chivers and Raemaekers (1980), Ellefson (1974),Geissmann (1991), Ibscher (1967), McKenna (1982),Miller (1997), Rumbaugh (1965, 1967), Smith et al.(1994), Smith and Jungers (1997), and records ofIndianapolis Zoo.

(Continued)

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES 213

APPENDIX B (Continued)

Genus and species Notes Sources

H. syndactylus Dental eruption schedule from Rumbaugh(1967) and Smith et al. (1994)

Fox (1984), Geissmann (1991), Miller (1997),Orgeldinger (1994), Rumbaugh (1967), Smith et al.(1994).

Pongo pygmaeus Dental eruption schedule from Smith et al.(1994) and Fooden and Izor (1983)supplemented by zoo records.

Fooden and Izor (1983), Galdikas (1985), Jungers(1988, 1997), Markham and Groves (1990), Markham(1994), Smith et al. (1994), Tobias (1994), Watts andPusey (1993), and records of Lowry Park ZoologicalGardens and Auckland Zoological Park.

Pan troglodytes Dental eruption schedule from Anemone et al.(1996), Conroy and Mahoney (1991), Fleagle(1998), Kuykendall et al. (1992), and Smith etal. (1994). Adult body masses are equallyweighted pooled subspecies values.

Anemone et al. (1996), Conroy and Mahoney (1991),Fleagle (1998), Goodall (1986), Graham et al. (1985),Hardin et al. (1975), Kuykendall et al. (1992), Nishidaet al. (1990), Pilbeam (1988), Pusey (1990), Ross (1991),Smith et al. (1994), Smith and Jungers (1997), Tobias(1994), Tutin (1994), Uehara and Nishida (1987); Wattsand Pusey (1993).

Gorilla gorilla Dental eruption schedule from Smith et al.(1994), Keiter (1981), and Willoughby (1978).Adult body masses are equally weightedpooled subspecies values.

Fossey (1979), Harcourt et al. (1981), Harvey et al.(1987), Jungers and Susman (1984), Keiter (1981),Smith et al. (1994), Smith and Jungers (1997), Tobias(1994), Watts (1991), Willoughby (1978).

214 L.R. GODFREY ET AL.

APPENDIX B (Continued)