Teeth, Brains, and Primate Life Histories

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 114:192214 (2001)
Teeth, Brains, and Primate Life Histories

Laurie R. Godfrey,1* K.E. Samonds,2 W.L. Jungers,2 and M.R. Sutherland3
Department of Anthropology, University of Massachusetts at Amherst, Amherst, Massachusetts 01003-4805 Department of Anatomical Sciences, School of Medicine, State University of New York at Stony Brook, Stony Brook, New York 11794-8081 3 Statistical Consulting Center, Graduate Research Center, University of Massachusetts at Amherst, Amherst, Massachusetts 01003-4535
2 1
KEY WORDS
dental development; diet; cranial capacity; life histories; primates taxa. What is the adaptive signicance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data afrm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses. Am J Phys Anthropol 114:192214, 2001.
ABSTRACT This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous
2001 Wiley-Liss, Inc.
Life history theory has grown enormously over the past several decades. Its focus has shifted away from body size as an explanation for the fast-slow continuum described by early theorists (Taylor, 1965; MacArthur and Wilson, 1967; Peters, 1983; Calder, 1984). Modern life history theory attempts to explain why strong correlations hold, across so many taxa, between body size, longevity, and so on. Environmental stability, adult mortality, and body size optimization have gured prominently in life history theory as it has developed over the past several decades (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 et al., 1994), dental development is not often considered in studies of life history variation. There are several reasons why dental development might be of great interest to students of mammalian life histories, however: 1) Dental development may provide an important key to understanding the ontogenetic acquisition of ecological competence in the life histories of primate species. Weanlings belonging to different primate species are not equally ecologically competent; the relationship between dental eruption and weaning may elucidate that variation. 2) The relative timing of aspects of skeletal and dental development may or may not be related in a predictable manner to body size or reproductive parameters that tend to describe the classic (fast-slow) life history continuum. 3) Dental development provides
a means through which life history inferences may be drawn for extinct species, as long as the relationship between dental development and life history variation among their extant relatives is well understood (Smith, 1989; Morbeck, 1997; Dirks, 1998; Reed et al., 1998; Kelley, 1999; Godfrey et al., in press, a). This requires detailed analyses of the adaptive signicance, in behavioral ontogenetic terms, of the timing of dental eruption. This paper explores the relationship between dental development and other variables (such as age at weaning, age at rst female breeding, body size, brain size) that are more commonly considered in studies of mammalian life history variation. Our task is not to test competing explanations of life history variation (i.e., the models of MacArthur and Wilson, 1967; Charnov, 1991, 1993; Kozlowski and Weiner, 1997). Such an endeavor would require consideration of birth and mortality rates for individuals in different life cycle stages across species (e.g., Ross and Jones, 1999). Rather, we are interested in body size, brain size, and diet as possible correlates of 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.
2001 WILEY-LISS, INC.
TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

TABLE 1. Samples of measured crania1 Family Indridae Genus and species Propithecus tattersalli Propithecus verreauxi Propithecus diadema Avahi laniger Varecia variegata Hapalemur griseus Lemur catta Eulemur macaco Eulemur fulvus Lepilemur rucaudatus Galago moholi Callithrix jacchus Saguinus nigricollis Saguinus fuscicollis Saimiri sciureus Cebus albifrons Cebus apella Aotus trivirgatus Alouatta palliata Alouatta caraya Ateles geoffroyi Chlorocebus aethiops Macaca fascicularis Macaca mulatta Macaca nemestrina Papio cynocephalus Papio anubis Kasi vetulus Semnopithecus entellus Trachypithecus franc oisi Trachypithecus cristata Trachypithecus obscura Nasalis larvatus Piliocolobus badius Colobus guereza Hylobates lar Hylobates syndactylus Pongo pygmaeus Pan troglodytes Gorilla gorilla Dietary category 3 3 3 3 2 2 2 2 2 3 1 1 1 1 1 2 2 2 3 3 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 2 3 2 2 3 Immature individuals 1 21 13 8 11 11 16 6 20 6 15 7 8 2 4 14 12 4 9 5 16 16 28 9 14 8 12 9 30 2 17 18 11 11 23 16 5 8 13 6
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Mature individuals 1 25 30 17 6 7 11 8 8 14 14 6 9 7 6 10 10 9 10 7 17 8 15 6 7 6 9 14 8 9 14 36 8 6 17 9 7 9 8 7
Lemuridae
Lepilemuridae Galagonidae Callitrichidae Cebidae
Atelidae Cercopithecidae
Hylobatidae Pongidae Hominidae

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 varying degrees.
our discussion to the postcanine teeth, as the timing of canine eruption may be affected by factors relating to the ontogeny of agonism, and should be considered in conjunction with studies of the evolution of sexual dimorphism. We tested six hypotheses that might explain variation in the pace of dental development in nonhuman primates. Two link development to aspects of adult size; four relate development to diet (food processing needs, the quality of the diet, or the spatiotemporal distribution and abundance of preferred food resources). Most of the hypotheses put forth here were constructed to explain variation in skeletal development and not the development of the dentition per se. Only the brain pleiotropy and food processing hypotheses make explicit predictions regarding dental development. Our hypotheses are not necessarily mutually exclusive, as some of our explanatory variables (folivory, relative brain size, amount of protein in the diet, and so on) are themselves correlated. Folivorous species might experience more rapid development than like-sized frugi-
vores as a corollary of more accelerated growth and skeletal maturation, earlier brain maturation, relatively small adult brain size, rapid acquisition of ecological independence, low intraspecic feeding competition, and/or the mechanical requirements for breaking down leaves and seeds. Insectivorous primates might experience rapid development as a corollary of their small brains, small bodies, and/or high protein diets. It is only through an examination of the complex interrelationships among possible explanatory variables that we can hope to understand dental developmental differences across the order Primates. MATERIALS AND METHODS Samples Dental eruption and metric data were collected by K.E.S. and L.R.G. on 900 individuals (465 immatures, and 435 adults) belonging to 40 species in 11 families of nonhuman primates (Table 1). Because there is little published information on the dental
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eruption schedules of folivorous primates or of lemurs in general, we supplemented the published data for these taxa with life history data inferred from unpublished museum and captive-animal records. Using specimens in museum collections in Europe, the United States, and Madagascar, we compiled known ages for zoo- or facility-raised individuals (whenever available), collection dates for wild-caught lemurs (whose reproductive synchrony allows biological age to be estimated for immature individuals with known death dates), coat characteristics for colobines and some New World monkeys (whose infant and/or juvenile coat color-change schedule allows age to be estimated for immature individuals with associated skins), and body masses of wild-caught and captive individuals belonging to species whose growth trajectories (mass increase over time) have been published. Also considered were the cranial dimensions of individuals of known ages. Combining these data with previously published data on dental eruption schedules, we were able to reconstruct at least partial dental eruption schedules for the primate species in our database (including 10 lemur species and 8 colobines). Life history data (age at weaning, age at rst female breeding, adult female body mass, adult female cranial capacity) were compiled from the primary literature. (Additional life history data compiled for the same set of species were included in multiple regression and principal components analyses reported elsewhere; Godfrey et al., in press, b). When values for adult female cranial capacity were unavailable, they were measured directly from museum specimens by one of the authors (W.L.J.). Adult female cranial capacities were used for all sexually dimorphic species and preferred for all species, although pooled-sex cranial capacities were used for some sexually monomorphic species, when necessary. For each individual in our database, we measured the mesiodistal and buccolingual diameters of the milk and permanent postcanine teeth. We then calculated species mean values for the adult postcanine occlusal area, as well as postcanine occlusal areas at two absolute ages (4 months and 1 year) and at weaning. Dental precocity was ascertained by counting the postcanine teeth erupted at 4 months, 1 year, and weaning (including the already-replaced milk teeth), and then constructing a ratio of postcanine teeth erupted at each age (or life-history stage) to the species-typical total number of postcanine teeth (deciduous plus permanent). Endowment at weaning was calculated by summing the average mesiodistal times buccolingual dimensions of all teeth present at weaning (excluding those already replaced), and calculating the ratio of postcanine occlusal area at weaning to the mean adult postcanine occlusal area (permanent teeth only). Dental precocity at 4 months and 1 year was used to assess how absolute rates of dental development vary independently of the degree of dental development at weaning. Ap-
pendix A provides our dental eruption data and key life history parameters. Appendix B lists the sources for these data. Dietary categories (insectivore, frugivore, folivore) were assigned on the basis of information in the primary literature, and diet was treated as a categorical variable (Table 1). A score of 1 (little or no foliage) was given to species consuming primarily insects and fruit (insectivores). A score of 2 (moderate foliage and ber) was given to species whose primary staple is fruit supplemented by leaves (frugivores). A score of 3 (high foliage and ber) was given to species whose primary staple is foliage and, to varying degrees, seeds (folivores). All anatomical or physiological as well as behavioral folivores were assigned to the latter category. Anatomical folivores consume fruit to varying degrees; brous, unripe fruit may be preferred over ripe fruit, and seeds are often chewed rather than swallowed whole or discarded. The diets of many primate species are affected by food availability and can change substantially between seasons or localities. Thus, despite the fact that colobus and leaf monkeys are all anatomical folivores, leaf consumption at different forests or in different seasons can vary from 47 82% (Piliocolobus badius), 4777% (Colobus guereza), 2751% (Colobus angolensis), and so on (see Kirkpatrick, 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 as 50% (Kirkpatrick, 1999). Conversely, anatomical frugivores sometimes consume enormous quantities of leaves. Living in the dry deciduous forests of western Madagascar, the western rufous lemur (Eulemur fulvus rufus) deviates markedly from the eastern rufous lemur (also E. f. rufus) and from all other Eulemur species, in consuming between 50 90% leaves (Sussman, 1974; Freed, 1999). In contrast, fruit makes up more than 65% of the diet of eastern rufous lemurs at all times, and foliage never exceeds 20% (Overdorff, 1993). Like other lemurids, E. f. rufus is not a seed predator (Overdorff and Strait, 1998). Future analyses of diet and life history variation should take into consideration such dietary plasticity. Data analysis Our rst task was to specify the predictions of each of our hypotheses, identifying shared as well as unique predictions. Shared and unique contributions of explanatory variables were then explored using correlation and partial correlation analysis. Partial correlations are a convenient way to accomplish essentially the same goal as multiple regression with more than one independent variable (Smith, 1999, and references therein). For example, we can ask if body mass variation explains a significant amount of variation in dental precocity above and beyond that explained by its covariation with cranial capacity; cranial capacity would be the variable controlled for in this case.

TABLE 2. Predictions of the competing hypotheses1 Prediction and hypothesis Adult & mass is negatively correlated with pace of dental development, even after controlling for effects of cranial capacity. Adult & cranial capacity is negatively correlated with absolute pace of dental development, even after controlling for effects of body size. Big-bodied species have weanlings that are less dentally advanced than those of small-bodied species. Big-brained species have weanlings that are less dentally advanced than those of small-brained species. Folivores exhibit faster dental development than do like-sized frugivores. Folivores wean their offspring earlier than do like-sized frugivores. Folivores reproductively mature earlier than do like-sized frugivores. Folivores exhibit more advanced dental development at weaning than do likesized frugivores. Big-brained species have weanlings that are less dentally advanced than those of small-brained species, controlling for effects of body size. Folivores have smaller brains than do like-sized frugivores. There is no difference between dental development at weaning of folivores and frugivores, controlling for cranial capacity and body size. Late maturers exhibit slower dental development than like-sized early maturers. Folivores exhibit faster dental development than do frugivores of similar brain size. Folivores exhibit more advanced dental development at weaning than do frugivores, controlling for effects of age at weaning. Folivores exhibit more advanced dental development at weaning than do frugivores, controlling for effects of brain size. Insectivores wean their offspring earlier than do like-sized frugivores. Insectivores exhibit faster dental development than do like-sized frugivores. Insectivores reproductively mature earlier than do like-sized frugivores.
1
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DCH X
BPH
FIH
RAH
FPH
PRH
X X2 X3 X4 X X X X X X X X X X X X X X X X X4 X X X X
DCH, design constraint hypothesis; BPH, brain pleiotropy hypothesis; FIH, foraging independence hypothesis; RAH, risk aversion hypothesis; FPH, food processing hypothesis; PRH, protein richness hypothesis. 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.
2
A problem that sometimes plagues cross-species studies is that of strong phylogenetic correlation (Felsenstein, 1985; Harvey and Pagel, 1991). Unless one can assume a starburst phylogeny (a bad assumption for primates), species cannot be treated as independent data points due to a nested hierarchy of relatedness. Closely related taxa are likely to be similar simply because they share a common ancestry. This phylogenetic inertia can result in spuriously narrow condence intervals and type I errors (Garland et al., 1992, 1999; Harvey and Purvis, 1991; Pagel, 1992), in part because degrees of freedom are grossly inated (Smith, 1994). We acknowledge and adjust for this potentially serious problem by using the variance components approach of Smith (1994) to calculate effective degrees of freedom from discounted sample sizes. We use the maximum likelihood solution to variance components available in SAS (procedure varcomp). To determine the effective N for partial correlation analysis, we followed the recommendation of Smith (1994), selecting the smaller of two choices: 1) the effective N calculated for the dependent variable; or 2) the mean of the effective Ns calculated for all variables. Elsewhere, and in a context different from the hypothesis testing done here, we report the results of multivariate treatments of phylogenetically independent contrasts (PICs) derived from our dental and life-history data (Godfrey et al., in press, b).
We wish to note that the results of our analyses of PICs are highly consistent with the results of the species-value analyses reported here. Table 2 summarizes the predictions of each of the six hypotheses and their corresponding statistical tests. The statistical signicance of correlations found in our analyses is assessed for both traditional and phylogenetically reduced degrees of freedom. The appreciable difference between our sample Ns and the calculated discounted Ns points to a nontrivial amount of phylogenetic constraint to most of our variables (Table 3). Working hypotheses are considered strongly supported whenever discounted as well as traditional degrees of freedom yield signicance at P 0.05. They are considered moderately supported whenever P 0.05 for traditional, but not discounted, degrees of freedom, and weakly supported when the signal is in the predicted direction, but signicance, even under traditional degrees of freedom, is marginal (P 0.1). Under other circumstances, working hypotheses are unsupported. Directional hypotheses (e.g., A B) are tested using one-tailed probabilities and null hypotheses of the form A B. When, occasionally, working hypotheses generate predictions in the form of nondirectional null hypotheses (A B), they are tested using two-tailed probabilities. Whereas the rationales of alternative dietary hypotheses differ, some of their predictions are shared. It is the unique
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TABLE 3. Effective or discounted sample sizes (after Smith, 1994) Variable All taxa (N 40) 12 10 21 11 11 9 11 18 22 Frugivores and folivores (N 35) 10 8 26 9 9 8 8 18 21 Insectivores and frugivores (N 22) 10 9 13 9 9 6 11 10 9
Log10 adult female mass Log10 adult cranial capacity Foliage consumption Age at weaning Age at rst breeding Dental precocity at 4 months Dental precocity at 1 year Dental precocity at weaning Dental endowment at weaning
predictions of each hypothesis that are most critical to hypothesis testing. HYPOTHESES The design constraint hypothesis (DCH) The design constraint hypothesis is grounded in the work of Taylor (1965), Western (1979), and other theorists who treated body size as developments engine. Its premise is that selection for changes in body mass will effect concomitant changes in life history parameters. In general, large-bodied species develop more slowly than small-bodied species (Peters, 1983; Calder, 1984). If dental development is a mere part and parcel of a size-driven developmental clock, then large-bodied species should also exhibit slow dental development. Adult mass should be negatively correlated with the pace of dental development, even after the effects of other variables such as cranial capacity are controlled. Furthermore, if adult body size is the primary determinant of the pace of dental development, then, regardless of diet, species that are small should exhibit high dental precocity at 4 months and 1 year. Diet should have little or no size-independent effect on dental development. Folivores might be expected to exhibit slower dental development than frugivores, and insectivores faster dental development than frugivores, but only to the extent that folivores tend to be larger and insectivores smaller in body size. The implications of the DCH for dental development at weaning depend on the relationship between weanling and maternal mass. Implicit in the work of Taylor (1965) is the notion that all life history events are scaled functions of body size. Charnov (1991, 1993) argued that weaning occurs when youngsters attain a xed proportion of maternal body size. However, Purvis and Harvey (1995) found that small-bodied ungulates and other mammals tend to have weanlings that are relatively large, and the ratio of weanling to maternal mass is inversely correlated with maternal mass. Whereas some have claimed that Charnovs xed-proportionality rule holds for anthropoid primates, we found that the generalization by Purvis and Harvey (1995) applies both for anthropoids alone and for anthropoids and
strepsirrhines combined.1 Because small-bodied primates tend to wean their offspring at an advanced state of growth and development, one might expect high dental precocity in the weanlings of small-bodied species. The brain pleiotropy hypothesis (BPH) A central role for the brain in mammalian growth and development has been defended by many researchers (reviewed in Ross and Jones, 1999). In mammals, lactation acts as a kind of buffer, protecting infants against the vicissitudes of the environment. Virtually all postnatal brain growth is complete at weaning (Martin, 1983). Species with large brains must extend the period of brain growth and delay weaning in order to accommodate the high energetic costs of growing large brains. The maternal energy hypothesis of Martin (1996) elaborates further on the notion that brain growth is central to reproduction: it is the mothers need to sustain brain growth (via lactation) which effectively sets the developmental clock (see also Lee, 1999). Cranial capacity should predict age at weaning and rst breeding. Smith (1989, 1992) argued for a link between brain and dental development. Dental development may be prolonged as an incidental effect of prolonged brain growth. If dental development is more closely tied to cranial capacity than to body size, then one should expect, even after controlling for the effects of body size, that small-brained species will develop more rapidly than large-brained creatures. Adult female cranial capacity should be inversely correlated with dental precocity at 4 months and 1 year. Because small-brained species should also wean their offspring at an early age, there is no necessary, logical connection between brain size and dental precocity or endowment at weaning. However, if weaning occurs at a relatively advanced stage of skeletal
1 On the basis of anthropoid data published by Lee et al. (1991), we found that the log10 of the ratio of weaning to maternal mass in primates is indeed inversely correlated with log10 maternal mass (r 0.54, N 30, one-tailed P 0.001). The relationship is even stronger when data for four lemurids and one indrid are included (r 0.60, N 35, one-tailed P 0.0001). Data from the Duke University Primate Center.
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growth and development in small-brained creatures, then weanlings of small species might also be expected to exhibit an advanced state of dental development. Again, diet should have little or no sizeindependent effect on dental development. Folivores might be expected to exhibit more rapid dental development than like-sized frugivores, but only to the extent that they tend to have smaller brains. The foraging independence hypothesis (FIH) Our foraging independence hypothesis is a logical derivative of what has been called the need to learn hypothesis (Ross and Jones, 1999), another hypothesis which purports to explain the observed correlation between large brain size and delayed reproduction. Its premise is that both large brains and late reproduction result from selection for prolonged learning (Gibson, 1986; Dunbar, 1992, 1995; Byrne, 1995; Joffe, 1997). Whether selection operates mainly to enhance social cognition or to enhance problem-solving in complex environments, a complex foraging support network for weanlings (with intergenerational transmission of particular foraging skills) may be options only for taxa with large brains. The trade-off is that, to sustain the social transmission of complex skills, highly encephalized species must also limit the number of offspring, delay weaning, extend juvenescence, and delay reproduction. Youngsters acquire foraging skills over an extended period of time, and inefcient weanlings can still survive with help from adults. This help comes in a variety of forms. Adults can set an example, engage in active pedagogy, defend food resources against conspecics, or transfer food directly to immature individuals (Fragaszy and Bard, 1997). For weanlings of poorly encephalized species, survival depends on greater self-sufciency. Greater dental development at weaning may compensate for a weak foraging-support network or for poor discrimination in food selection by weanlings. Thus, high dental precocity and endowment at weaning may be selectively advantageous for species with relatively low levels of peri- and postweaning maternal investment and weak foraging-support networks. The foraging independence hypothesis yields a number of predictions, only three of which are unique to it alone (see Table 2). The unique predictions of the FIH are: 1) highly encephalized species should have weanlings that are less advanced dentally than those of poorly encephalized species (i.e., controlling for the effects of body size, cranial capacity should be negatively correlated with dental development at weaning); 2) because they do not need to acquire complex foraging skills, folivores should have smaller brains than like-sized frugivores; and 3) folivores should exhibit greater dental precocity and endowment at weaning than like-sized frugivores only to the extent that they have relatively smaller brains and less complex social interactions.
There is no reason to expect any differences between the dental precocities of folivores and frugivores at weaning once the effects of both cranial capacity and body size have been controlled. Predictions common to this and some other hypotheses are: 1) if weaning is early and if dental development at weaning is more advanced in folivores than in like-sized frugivores, then dental development should be more rapid (on an absolute scale) in folivores than in like-sized frugivores; 2) because they do not need as extended a period of time to learn foraging skills, folivores should wean their offspring earlier than like-sized frugivores; 3) given the shorter period required for skill acquisition in folivores, folivores should exhibit earlier reproductive maturation than like-sized frugivores; and nally, 4) due to the smaller group sizes and less complex social interactions of folivores, newly weaned folivores should be more advanced dentally than newly weaned, likesized frugivores. The risk aversion hypothesis (RAH) The premise of the risk aversion hypothesis is that resource distribution and abundance covary with diet, and affect the risk of starvation (Janson and van Schaik, 1993; Leigh, 1994). Due to higher intraspecic competition for scarce resources, juveniles living in risky environments will be more likely to die of starvation than juveniles living in low-risk environments. Slower growth reduces the probability of starvation, and is therefore favored by selection for species exploiting risky food resources. Some researchers have noted that the RAH is hard to test because the degree to which resources are actually limiting is often difcult to measure (Watts and Pusey, 1993). However, Leigh (1994) defended the RAH, using broad comparisons of folivorous and frugivorous anthropoids, on the explicit presumption that the foods exploited by frugivores are riskier than those eaten by folivores (Janson and van Schaik, 1993). Leigh (1994) used growth curves to test this hypothesis; the predictions of the RAH for dental development were not tested. The sole unique prediction of the RAH is that the absolute rate of dental development should be inversely correlated with age at rst breeding; late maturers should develop slowly (Table 2). In addition, if the key to reduced predation mortality is rapid growth and maturation, folivores might be expected to wean their young at an earlier age, and to mature earlier than species relying on less predictable food resources. Rapid dental development should characterize folivores, but there is no reason to expect advanced dental development at weaning, because dental precocity at weaning is not the target of selection, and because weaning should also be early. The food processing hypothesis (FPH) The premise of the food processing hypothesis is that the mechanical requirements of mastication co-
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Yes, moderately 0.31 40 (14) 0.025 (0.133) Working hypothesis supported? Yes, strongly 0.000 (0.006) 0.77 40 (9) Yes, strongly 0.69 40 (11) 0.000 (0.008)
TABLE 4. Test of design constraint and brain pleiotropy hypotheses, with effective Ns and probabilities under discounting in parentheses1
Big-bodied species have weanlings that are less dentally advanced than weanlings of small-bodied species. Adult & cranial capacity is negatively correlated with pace of dental development, even after controlling for effects of body size.
The premise of the protein richness hypothesis is that, because protein is essential for growth, the relative amount of protein in the diet inuences rates of growth and development (Glander, 1980; Froehlich et al., 1981). Species with diets high in protein should experience rapid dental eruption as a corollary of rapid overall growth and maturation. Leaves, seeds, and insects are high in protein, and might facilitate rapid growth. A caveat is that the main staple in the diet is not necessarily a good indicator of the quality of the diet. As Wright (1999) notes, whereas anthropoid folivore milk is higher in protein content than that of anthropoid frugivores, the same is not the case for folivorous vs. frugivorous lemurs. If protein consumption is the primary determinant of rate of development, then folivores, seed predators, and insectivores might be expected to develop and mature more rapidly than frugivores of comparable adult body size. This hypothesis makes no prediction regarding dental development at weaning, but it does predict early weaning and rst
Working hypothesis
DCH
BPH
Big-brained species have weanlings that are less dentally advanced than weanlings of small-brained species.
The protein richness hypothesis (PRH)
DCH, design constraint hypothesis; BPH, brain pleiotropy hypothesis.
vary with diet. According to this hypothesis, selection must prepare weanlings to process those solid foods available to them at weaning or shortly thereafter (Eaglen, 1985). Dental endowment and precocity at weaning will therefore depend on the mechanical requirements for processing those foods. This hypothesis predicts that dental development at weaning is directly targeted by selection. Folivorous weanlings need to be better equipped than frugivorous weanlings, not only because they must break down highly brous sheetlike foods, but because they tend to masticate (rather than discard or swallow whole) seeds (Dew and Wright, 1998; Hemingway, 1996, 1998; Kirkpatrick, 1999; Overdorff and Strait, 1998). Differences in the morphology of the permanent cheek teeth of folivores and frugivores have been studied in detail (Covert, 1986; Jungers et al., in press; Kay, 1978; Yamashita, 1998a,b). Folivores have molars with relatively higher and longer shearing blades and larger crushing basins. The FPH predicts that diet directly inuences dentition at weaning. This inuence should be independent of age at weaning, brain size, or body size. Unless age at weaning is delayed in folivores, the dentitions of folivores and seed predators might be expected to develop faster (on an absolute scale) than those of frugivores. Thus, folivores might be expected to exhibit faster dental development than frugivores of similar body size. The unique predictions of the FPH are that: 1) folivores should exhibit faster dental development on an absolute scale than frugivores of similar brain size; 2) with age at weaning controlled, folivores should exhibit more advanced dental development at weaning than frugivores; and 3) with brain size controlled, folivores should exhibit more advanced dental development at weaning than frugivores.
No
Test of null hypothesis with P values
0.999 (0.921)
No 0.997 (0.903) 40 (11) 0.43
N (N eff.)
r or partial r
40 (9)
Log cranial capacity Log cranial capacity
Controlled variable
0.17
0.52
40 (14)
0.147 (0.276)
No
Explanatory variable
Dental precocity at 4 months Dental precocity at 1 year Dental precocity at weaning Adult & mass is negatively correlated with pace of dental development, even after controlling for effects of cranial capacity.
Predictions of working hypothesis
Dental precocity at 4 months Dental precocity at 1 year Dental precocity at weaning
Dependent variable
Log cranial capacity Log cranial capacity Log cranial capacity
Log adult & mass Log adult & mass Log adult & mass
Log adult & mass Log adult & mass
TABLE 5. Test for the foraging independence hypothesis (unique predictions in bold)
Predictions of working hypothesis Log adult & mass 0.61 0.50 0.35 35 (9) 35 (9) 35 (18) 35 (19) 0.52 0.31 0.66 0.14 40 (13.33) 40 (14.67) 35 (8) 35 (15.5) 0.32 0.45 0.32 35 (8) 35 (8) Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass and log cranial capacity Log adult & mass and log cranial capacity
Dependent variable
Explanatory variable Controlled variable Partial r N (N eff.)
Test of null hypothesis with P values 0.000 (0.056) 0.001 (0.110) 0.013 (0.185) 0.030 (0.208) 0.003 (0.030) 0.000 (0.092) 0.000 (0.032) 0.025 (0.137) 0.000 (0.038) 0.434 (0.633)
Working hypothesis supported? Yes, moderately Yes, moderately Yes, moderately Yes, moderately Yes, strongly Yes, moderately Yes, strongly Yes, moderately Yes, strongly Yes, cannot reject null hypothesis
Folivores exhibit faster dental development than do like-sized frugivores.
Dental precocity at 4 months Dental precocity at 1 year Age at weaning Age at & rst breeding Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Log cranial capacity Log cranial capacity Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Dental precocity at weaning Dental endowment at weaning Dental precocity at weaning Dental endowment at weaning Log adult & cranial capacity Dental precocity at weaning Dental endowment at weaning
Folivores wean their offspring earlier than do like-sized frugivores. Folivores reproductively mature earlier than do like-sized frugivores. Folivores exhibit more advanced dental development at weaning than do like-sized frugivores.
Diet: vs. Diet: vs. Diet: vs.
frugivores folivores frugivores folivores frugivores folivores
Big-brained species have less advanced weanlings than small-brained species, controlling for effects of body size. Folivores have smaller brains than do like-sized frugivores. Folivores and frugivores exhibit no difference in dental development at weaning, when effects of both cranial capacity and body size are controlled (test is two-tailed).
0.10
35 (16.25)
0.578 (0.726)
Yes, cannot reject null hypothesis
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Yes, moderately Yes, moderately Yes, moderately Yes, moderately Working hypothesis supported?
breeding in species with high protein diets (once body size is controlled). Its unique predictions pertain to comparisons between insectivores and frugivores (Table 2). RESULTS Let us consider each of our hypotheses in light of our data. The brain pleiotropy hypothesis does considerably better than the design constraint hypothesis at explaining variation in dental development among primates (Table 4). Adult body size fares poorly in comparison to cranial capacity when used to predict the pace of dental development. It is only because adult body mass is correlated with other traits (cranial capacity) that are more strongly linked to dental development that it predicts the pace of dental development at all. Cranial capacity is the best predictor of dental precocity at 4 months and 1 year, as anticipated by Smith et al. (1994). The shared predictions of the four dietary hypotheses tend to be moderately or strongly supported (Tables 5 8). The unique predictions of the foraging independence hypothesis are also well supported by the data (Table 5). They are that folivores have smaller brains than like-sized frugivores, and that, once the effects of both cranial capacity and body size have been removed, there will be no difference between the dentitions of folivores and frugivores at weaning. Lemurs comprise an apparent exception to the latter rule, however. Folivorous lemurs exhibit greater precocity at weaning than do frugivorous lemurs, even after controlling for both brain and body size (partial correlation 0.69, one-tailed P 0.019, N 10). This sample is too small to undergo meaningful discounting. The unique predictions of the risk aversion hypothesis are not supported by our data (Table 6). There is little or no connection between age at rst breeding and the pace of dental development, once the effects of body size are controlled. The predicted link between the pace of reproductive and ecological (dental) maturation is not supported by our data. Furthermore, the RAH cannot account for the observed high dental precocity and endowment of folivores at weaning. Clearly, dental developmental acceleration is not solely part and parcel of a general acceleration of growth and development in folivores. The food processing hypothesis, that the mechanical requirements for food processing affect dental development at weaning, is well supported by our data (Table 7). Folivorous weanlings tend to have high dental precocity and endowment, particularly when compared to like-sized, more frugivorous relatives. The unique predictions of the FPH (rst, that folivore/seed predators will exhibit faster dental development than frugivores of similar brain size; and second, that with age at weaning controlled, folivore/ seed predators will exhibit more advanced dental development at weaning) are supported by our data. The protein richness hypothesis, that the pace of development depends on the amount of protein in
No 0.195 (0.365) 0.14 40 (9)
TABLE 6. Test of the risk aversion hypothesis (unique predictions in bold)
Partial r
0.35
Dental precocity at 4 months Dental precocity at 1 year Age at weaning
Folivores wean their offspring earlier than likesized frugivores. Folivores reproductively mature earlier than like-sized frugivores. Late maturers exhibit slower (dental) development than like-sized early maturers.
Age at rst breeding Dental precocity at 4 months Dental precocity at 1 year
Dependent variable
Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Age at rst breeding Age at rst breeding
Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass
Controlled variable
0.32
0.09
0.61
0.50
40 (11)
N (N eff.)
35 (8)
35 (8)
35 (9)
35 (9)
0.292 (0.362)
0.000 (0.056)
0.001 (0.110)
0.013 (0.185)
0.030 (0.208)
No
TABLE 7. Test of food processing hypothesis (unique predictions in bold)
Predictions of working hypothesis 0.61 0.50 0.45 0.32 0.46 0.36 0.46 0.33 0.41 Log cranial capacity 0.26 35 (18) 35 (19) 35 (8) 35 (8) 35 (17.67) 35 (18.67) 35 (17.33) 35 (18.33) 35 (8) 35 (8)
Dependent variable Partial r N (N eff.)
Controlled variable
Test of null hypothesis with P values 0.000 (0.056) 0.001 (0.110) 0.003 (0.030) 0.000 (0.092) 0.003 (0.133) 0.017 (0.200) 0.003 (0.029) 0.026 (0.088) 0.007 (0.049) 0.066 (0.149)
Working hypothesis supported? Yes, moderately Yes, moderately Yes, strongly Yes, moderately Yes, moderately Yes, moderately Yes, strongly Yes, moderately Yes, strongly Yes, weakly
Folivores exhibit more advanced dental development at weaning than do like-sized frugivores.
Folivores exhibit faster dental development than do frugivores of similar brain size. Dental precocity at 1 year Dental precocity at weaning Dental endowment at weaning Dental precocity at weaning Dental endowment at weaning Age at weaning Age at weaning Log cranial capacity Log cranial capacity
Dental precocity at 4 months Dental precocity at 1 year Dental precocity at weaning Dental endowment at weaning Dental precocity at 4 months
Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log cranial capacity
Folivores exhibit more advanced dental development at weaning than do frugivores, controlling for age at weaning.
Folivores exhibit more advanced dental development at weaning than do frugivores of similar brain size.
Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores
202
Yes, moderately Yes, moderately Yes, moderately Yes, moderately Working hypothesis supported?
L.R. GODFREY ET AL.
Folivores wean their offspring earlier than do like-sized frugivores. Folivores reproductively mature earlier than do like-sized frugivores. Insectivores wean their offspring earlier than do like-sized frugivores. Insectivores reproductively mature earlier than do like-sized frugivores. Insectivores exhibit faster dental development than do like-sized frugivores.
the diet, receives mixed support (Table 8). On the one hand, it is generally true that species feeding on large amounts of insects, seeds, or foliage develop quickly. However, these species are also typically either small-bodied or small-brained. The unique predictions of the PRH are poorly supported by our data. Against expectations, controlling for the effects of body size, insectivores do not wean their offspring earlier than frugivores. Also against expectations, controlling for body size, there is no indication that insectivores mature earlier than frugivores. The prediction that insectivores should exhibit faster dental development (on an absolute scale) than like-sized frugivores receives equivocal support. An important consideration is the special role of age at weaning. Whereas age at weaning is better predicted by brain than by body size, it remains signicantly correlated with age at rst breeding, even after the effects of both log brain and log body size are controlled.2 It appears that selection can effect changes in the timing of reproductive events that are independent of size. It can also alter the plasticity of reproductive timing. In some species, weaning is sharply constrained phenologically (re lemurs, see Sauther, 1991; Wright, 1997, 1999). In others, weaning is far less constrained. A case in point is Pongo pygmaeus. Its age at weaning has been 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 precisely dened as the transition from life-sustaining to incidental dependency on the mother, its timing can be plastic (discussed in Lee, 1966, 1999). Weaning and reproductive maturation are affected by extrinsic variables (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 been exploring here. As might be expected (given the positive correlation between age at weaning and brain or body size, and the negative correlation between age at weaning and the pace of dental development), the ratio of dental development at weaning to age at weaning covaries inversely with brain and body size in primates (Fig. 1). Its correlation with cranial capacity is far tighter than that with body size. What is of interest to us here is the tendency for folivores in diverse clades to exhibit higher values for this ratio
0.996 (0.931)
0.989 (0.900)
0.552 (0.521) 0.03 22 (6)
TABLE 8. Test of protein richness hypothesis (unique predictions in bold)
Partial r
0.54
0.48
Dental precocity at 4 months Dental precocity at 1 year Age at weaning
Age at rst breeding Dental precocity at 4 months Dental precocity at 1 year
Age at rst breeding Age at weaning
Dependent variable
Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: frugivores vs. folivores Diet: insectivores vs. frugivores Diet: insectivores vs. frugivores Diet: insectivores vs. frugivores Diet: insectivores vs. frugivores
Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass Log adult & mass
Controlled variable
0.38
0.35
0.32
0.61
0.50
22 (11)
N (N eff.)
22 (9)
22 (9)
35 (8)
35 (8)
35 (9)
35 (9)
0.040 (0.129)
0.000 (0.056)
0.001 (0.110)
0.013 (0.185)
0.030 (0.208)
Yes, moderately
No
No
No
2 Partial correlation 0.88, N 40, one-tailed P 0.0001 with 36 degrees of freedom; Neff. 11, P 0.001 with 7 degrees of freedom.
Fig. 1. a: Scatterplot of log10 (dental precocity at weaning/age at weaning) vs. log10 (adult female mass). Triangles are insectivores, squares are frugivores, and circles are folivores (solid circles are Indridae). b: Scatterplot of log10 (dental precocity at weaning/age at weaning) vs. log10 (adult female cranial capacity). Triangles are insectivores, squares are frugivores, and circles are folivores (solid circles are Indridae).
Fig. 1.
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than do closely related frugivores. This difference is not a function of body size (Fig. 1a); and as particularly high positive transpositions for the leaf- and seed-eating Indridae demonstrate (Fig. 1b), it is not entirely a function of brain size. Finally, we note that, whereas folivores tend to exhibit greater dental endowment as well as greater precocity at weaning than do like-sized frugivores, the signal tends to be stronger for precocity than for endowment. Because the milk dentitions of frugivores must be functional over a longer period of time, and because the milk teeth of frugivores form in relatively larger jaws (due to their relatively retarded eruption schedule), the milk teeth of frugivores 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 regarding the absolute pace of dental development, i.e., that dental development will be rapid in species that exhibit: 1) small adult body size (design constraint hypothesis); 2) low cranial capacity (brain pleiotropy hypothesis); 3) rapid acquisition of foraging independence, coupled with low encephalization, and low peri- and postweaning parental investment (foraging independence hypothesis); 4) a low risk of starvation due to intraspecic competition for food resources, coupled with a relatively high risk of juvenile mortality due to predation (risk aversion hypothesis); 5) a diet that is high in brous leafy material and/or seeds, and requiring extensive processing (food processing hypothesis); and 6) a diet that is rich in protein (protein richness hypothesis). Several of these hypotheses also predict high dental endowment and precocity in folivores at weaning. They thus converge in predicting accelerated dental development in folivores on both absolute and relative scales. Our data show that brain size is a better predictor of dental development than body size. However, they also afrm the insufciency of cranial capacity as a predictor of dental development; the complexity of the absolute and relative pace of dental development in primates is more than any single factor can bear. In particular, we found that diet affects the absolute pace of dental development, independent of body size, age at rst breeding, and cranial capacity. Folivores generally have more accelerated dental developmental schedules than do comparably sized frugivores. But their accelerated dental development is not a mere consequence of a general pattern of life history acceleration in more folivorous taxa. Dental development in folivorous species also tends to be more advanced at weaning. Neither cranial capacity nor body size alone can account for the variation in the absolute or relative pace of dental eruption across all primate taxa. The advanced state of the dentitions of folivores at weaning (with variation in size and age at weaning controlled) suggests
that the state of dental development at weaning can be the direct target of selection; the mechanics of food processing may have an important effect on dental ontogeny. In general, our data offer the strongest support for the foraging independence and the food processing hypotheses, and equivocal support for the other dietary hypotheses. The (perhaps different) contributions of learning, food processing, and environmental risk to dental development in members of diverse primate clades are certainly worthy of future investigation. ACKNOWLEDGMENTS This project would not have been possible without the assistance of numerous people. For help in supplying specimens or unpublished data, we are indebted to David Archibald, Jacqui Bowman, G. Gray Eaton, Jack Fooden, Kenneth Glander, Christina Grassi, David Haring, Claire Hemingway, Mitchell Irwin, Karin Isler, Stephen King, Steven Leigh, Lawrence Martin, Robert Martin, Leanne Nash, Sheila OConnor, J. Michael Plavcan, Alison Richard, Elwyn Simons, Chia Tan, Michael Van Patten, and Patricia Wright. Data were compiled from the records of and/or specimens at the following facilities: American Museum of Natural History, New York; Anthropologisches Institut und Museum, Zurich; Aukland Zoological Park; California Primate Research Center, Davis; Columbus Zoological Garden; Dallas Zoo; Department of Anthropology, University of Massachusetts, Amherst; Duke University Primate Center; Field Museum of Natural History, Chicago; Hogle Zoo of Utah; Houston Zoological Gardens; Laboratoire de Pale ontologie des Verte bre s, Universite dAntananarivo, Madagascar; Laboratoire de Zoologie, Muse um National dHistoire Naturelle, Paris; Lowry Park; Museum of Comparative Zoology at Harvard University; Nationaal Natuurhistorisch Museum, Leiden; Natural History Museum, London; Oregon Regional Primate Center; Parc Ivoloina; Parc Tsimbazaza; Pittsburgh Zoo; Ranomafana National Park; San Diego State University; San Diego Zoo; State University of New York at Stony Brook; Smithsonian Institution; Woodland Park Zoological Gardens; and the Yerkes Regional Primate Center. This research was supported in part by NSF GER 9450175 to L.R.G., and NSF SBR9630350 to Elwyn Simons and the Statistical Consulting Center of the University of Massachusetts. Special thanks are owed to the curators of collections, anonymous reviewers, and Darren Godfrey, who produced Figure 1. LITERATURE CITED
Albignac R. 1981. Variabilite dans lorganisation territoriale et le cologie de Avahi laniger (le murien nocturne de Madagascar). C R Acad Sci [III] 292:331334. Anemone RL, Mooney MP, Siegel MI. 1996. Longitudinal study of dental development in chimpanzees of known chronological age: implications for understanding age at death of Plio-Pleistocene hominids. Am J Phys Anthropol 99:119 133.

Ayers JMC. 1986. Uakaris and Amazonian ooded forest. Ph.D. dissertation. University of Cambridge. Baldwin JD. 1985. The behavior of squirrel monkeys (Saimiri) in natural environments. In: Rosenblum LA, Coe CL, editors. Handbook of squirrel monkey research. New York: Plenum Press. p 3553. Baldwin JD, Baldwin JI. 1981. The squirrel monkey, genus Saimiri. In: Coimbra-Filho AF, Mittermeier RA, editors. Ecology and behavior of neotropical primates, volume 1. Rio de Janeiro: Academia Brasileira de Ciencias. p 277330. Bauchot R, Stephan H. 1966. Donne es nouvelles sur lence phalisation des insectivores et des prosimiens. Mammalia 30:160 196. Bentley-Condit VK, Smith EO. 1997. Female reproductive paramaters of Tana River yellow baboons. Int J Primatol 18:581 596. Bernstein IS. 1968. The lutong of Kuala Selangor. Behaviour (Leiden) 32:116. Boinski S. 1987. Birth synchrony in squirrel monkeys (Saimiri oerstedi): a strategy to reduce neonatal predation. Behav Ecol Sociobiol 21:393 400. Brandon-Jones D. 1985. Colobus and leaf monkeys. In: MacDonald D, editor. Primates. New York: Torstar Books. p 102 112. Brockman DK, Willis MS, Karesh WB. 1987. Management and husbandry of ruffed lemurs, Varecia variegata, at the San Diego Zoo. II. Reproduction, pregnancy, parturition, litter size, infant care and reintroduction of hand-raised infants. Zoo Biol 6:343369. Butynski TM. 1988. Guenon birth seasons and correlates with rainfall and food. In: Gautier-Hion A, Bourlie ` re F, Gautier JP, Kingdon J, editors. A primate radiation: evolutionary biology of the African guenons. Cambridge: Cambridge Univ. Press. p 284 322. Byrne RW. 1995. Primate cognition: comparing problems and skills. Am J Primatol 37:127141. Calder WA III. 1984. Size, function, and life history. Cambridge, MA: Harvard University Press. Carpenter R. 1935. Behavior of the red spider monkeys in Panama. J Mammal 16:171180. Cartmill M, Brown K, Eaglen R, Anderson DE. 1979. Handrearing twin ruffed lemurs Lemur variegatus at the Duke University Primate Center. Int Zoo Yrbk 19:258 261. Chapman C. 1987. Flexibility in diets of three species of Costa Rican primates. Folia Primatol (Basel) 49:90 105. Charnov EL. 1991. Evolution of life history variation among female mammals. Proc Natl Acad Sci USA 88:1134 1137. Charnov EL. 1993. Life history invariants: Some explorations of symmetry in evolutionary ecology. Oxford: Oxford University Press. Chase JE, Cooper RW. 1969. Saguinus nigricollis: physical growth and dental eruption in a small population of captiveborn individuals. Am J Phys Anthropol 30:111116. Chivers DJ, Raemaekers JJ. 1980. Long-term changes in behavior. 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 of infants in a free-ranging group of howling monkeys (Alouatta palliata). Folia Primatol (Basel) 54:115. Colquhoun IC. 1993. The socioecology of Eulemur macaco: a preliminary report. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum. p 1124. Conroy G, Mahoney CJ. 1991. Mixed longitudinal study of dental emergence in the chimpanzee, Pan troglodytes (Primates, Pongidae). Am J Phys Anthropol 86:243254. Covert HH. 1986. Biology of early Cenozoic primates. In: Swindler DR, Erwin J, editors. Comparative primate biology volume 1: systematics, evolution, and anatomy. New York: A.R. Liss. p 335359. Crandall LS. 1964. The management of wild animals in captivity. Chicago: University of Chicago Press.
205
Curtin SH, Chivers DJ. 1978. Leaf-eating primates of peninsular Malaysia: the siamang and the dusky leaf-monkey. In: Montgomery GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press. p 441 464. Dew JL, Wright PC. 1998. Frugivory and seed dispersal by four species of primates in Madagascars eastern rain forest. Biotropica 30:425 437. Dirks W. 1998. Histological reconstruction of dental development and age at death in a juvenile gibbon (Hylobates lar). J Hum Evol 35:411 425. Doyle GA. 1979. Development of behavior in prosimians with special reference to the lesser bushbaby, Galago senegalensis moholi. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 158 206. Dunbar RIM. 1992. Neocortex size as a constraint on group size in primates. J Hum Evol 22:469 494. Dunbar RIM. 1995. Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28:287296. Eaglen RH. 1985. Behavioral correlates of tooth eruption in Madagascar lemurs. Am J Phys Anthropol 66:307315. Eisenberg JF. 1981. The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. Chicago: University of Chicago Press. Eisenberg JF. 1989. Order Primates. In: Mammals of the neotropics. Volume 1. The northern neotropics: Panama, Colombia, Venezuela, Guyana, Suriname, French Guiana. Chicago: University of Chicago Press. p 233261. Eley RM, Strum SC, Muchemi G, Reid GDF. 1989. Nutrition, body condition, activity patterns, and parasitism of free-ranging baboons (Papio anubis) in Kenya. Am J Primatol 18:209 219. Ellefson JO. 1974. A natural history of white-handed gibbons in the Malayan peninsula. In: Rumbaugh DM, editor. Gibbon and siamang, volume 3. Basel: Karger. p 1136. Epple G. 1970. Maintenance, breeding and development of marmoset monkeys (Callithricidae) in captivity. Folia Primatol (Basel) 13:48 62. Fedigan L, Rose L. 1995. Interbirth intervals in sympatric monkeys in Central America. Am J Primatol 15:235245. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125:115. Fleagle JG. 1998. Primate adaptation and evolution, 2nd ed. New York: Academic Press. Fleagle JG, Mittermeier RA. 1980. Locomotor behavior, body size, and comparative ecology of seven Surinam monkeys. Am J Phys Anthropol 52:301314. Fleagle JG, Schafer M. 1982. Development and eruption of the mandibular cheek-teeth in Cebus albifrons. Folia Primatol (Basel) 38:158 169. Foerg R. 1982. Reproductive behaviour in Varecia variegata. Folia Primatol (Basel) 38:108 121. Fooden J. 1975. Taxonomy and evolution of liontail and pigtail macaques (Primates: Cercopithecidae). Fieldiana Zool 67:1 169. Fooden J. 1995. Systematic review of southeast Asian longtail macaques, Macaca fascicularis (Rafes, 1821). Fieldiana Zool NS 81:1206. Fooden J, Izor RJ. 1983. Growth curves, dental emergence norms, and supplementary morphological observations in known-age captive orangutans. Am J Primatol 5:285301. Fossey D. 1979. Development in the mountain gorilla (Gorilla gorilla 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, Chivers DJ, Brockelman WY, Creel N, editors. The lesser apes: evolutionary and behavioural biology. Edinburgh: Edinburgh University Press. p 324 332. Fragaszy D, Adams-Curtis L. 1997. Developmental changes in manipulation in tufted capuchins (Cebus apella) from birth through 2 years and their relation to foraging and weaning. J Comp Psychol 111:201211. Fragaszy DM, Bard K. 1997. Comparison and development and life history in Pan and Cebus. Int J Primatol 18:683701.
206
L.R. GODFREY ET AL.

Haddidian J, Bernstein IS. 1979. Female reproductive cycles and birth data from an Old World monkey colony. Primates 20:429 442. Hall RD, Beattie RJ, Wyckoff GH Jr. 1979. Weight gains and sequence of dental eruptions in infant owl monkeys (Aotus trivirgatus). In: Ruppenthal GC, editor. Nursery care of nonhuman primates. New York: Plenum Press. p 321328. Harcourt AH, Stewart KJ, Fossey D. 1981. Gorilla reproduction in the wild. In: Graham CE, editor. Reproductive biology of the great apes. New York: Academic Press. p 265279. Harcourt CS, Bearder SK. 1989. Comparison of Galago moholi in southern Africa with Galago zanzibaricus in Kenya. Int J Primatol 10:35 45. Hardin CJ, Liebherr G, Fairchild O. 1975. Articial insemination in chimpanzees Pan troglodytes. Int Zoo Yrbk 15:132134. Hartwig WC. 1996. Perinatal life history traits in New World monkeys. Am J Primatol 40:99 130. Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford: University of Oxford Press. Harvey PH, Purvis A. 1991. Comparative methods for explaining adaptations. Nature 351:619 624. Harvey PH, Martin RD, Clutton-Brock TH. 1987. Life histories in comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 181196. Hearn JP. 1982. The reproductive physiology of the common marmoset Callithrix jacchus in captivity. Int Zoo Yrbk 22:138 143. Hemingway CA. 1996. Morphology and phenology of seeds and whole fruit eaten by Milne-Edwards sifaka, Propithecus diadema edwardsi, in Ranomafana National Park, Madagascar. Int J Primatol 17:637 659. Hemingway CA. 1998. Selectivity and variability in the diet of Milne-Edwards sifakas (Propithecus diadema edwardsi). Implications for folivory and seed-eating. Int J Primatol 19:355 377. Hernandez-Camacho J, Deer TR. 1985. Some aspects of the conservation of non-human primates in Colombia. Primate Conserv 6:4250. 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 of primates in captivity. Ceylon J Sci [B] 20:369 389. Hladik CM. 1977. A comparative study of the feeding strategies of two sympatric species of leaf monkey: Presbytis senex and Presbytis 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 of colobus monkeys Colobus guereza, proboscis monkeys Nasalis larvatus and Douc langurs Pygathrix nemaeus in zoos. Int Zoo Yrbk 13:185188. Horwich R. 1974. Development of behaviors in a male spectacled langur. Primates 15:151178. Horwich R, Manski D. 1975. Maternal care and infant transfer in two species of colobus monkeys. Primates 16:49 73. Hrdlic ka A. 1925. Weight of the brain and of the internal organs in American monkeys. Am J Phys Anthropol 8:210 211. Hrdy SB. 1980. The langurs of Abu: female and male strategies of reproduction. Cambridge, MA: Harvard University Press. Hurme VO, van Wagenen G. 1953. Basic data on the emergence of deciduous teeth in the monkey (Macaca mulatta). Proc Am Philos Soc 105:105140. Ibscher L. 1967. Geburt und fru he Entwicklung zweier Gibbons (Hylobates lar l.). Folia Primatol (Basel) 5:43 69. Iwamoto M, Hamada Y, Watanabe T. 1984. Eruption of permanent teeth in Japanese monkeys (Macaca fuscata). J Anthropol Soc Nippon 92:273279. Izard MK, Nash L. 1988. Contrasting reproductive parameters in Galago senegalensis braccatus and G. s. moholi. Int J Primatol 9:519 527.
Freed BZ. 1999. An introduction to the ecology of daylight-active lemurs. In: Dolhinow P, Fuentes A, editors. The nonhuman primates. Mountain View, CA: Mayeld Publishing Co. p 123 132. Froehlich JW, Thorington RW Jr, Otis JS. 1981. The demography of howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Int J Primatol 2:207236. Galdikas BMF. 1985. Subadult male orangutan sociality and reproductive 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 dental eruption in Bolivian captive-born squirrel monkeys (Saimiri sciureus). Am J Primatol 8:195204. Garbutt N. 1999. Mammals of Madagascar. New Haven: Yale University Press. Garland T Jr, Harvey PH, Ives AR. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18 32. Garland T Jr, Midford PE, Ives AR. 1999. An introduction to phylogenetically based statistical methods, with a new method for condence intervals on ancestral values. Am Zool 39:374 388. Geissmann T. 1991. Age of maturation of siamangs. Am J Primatol 23:1122. Gest TR, Siegel MI. 1983. The relationship between organ weights and body weights, facial dimensions, and dental dimensions in a population of olive baboons (Papio cynocephalus anubis). Am J Phys Anthropol 61:189 196. Gibson D, Chu E. 1992. Management and behaviour of Franc ois langur Presbytis franc oisi franc oisi at the Zoological Society of San Diego. Int Zoo Yrbk 31:184 191. Gibson KR. 1986. Cognition, brain size and the extraction of embedded food resources. In: Else J, Lee PC, editors. Primate ontogeny, cogntion and social behavior. Cambridge: Cambridge University Press. p 93104. Glander KE. 1980. Reproduction and population growth in freeranging mantled howling monkeys. Am J Phys Anthropol 53: 2536. Glander KE, Fedigan LM, Fedigan L, Chapman C. 1991. Field methods for capture and measurement of three monkey species in 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 species from southeastern Madagascar. J Hum Evol 22:117. Godfrey LR, Petto AJ, Sutherland MR. In press, a. Dental ontogeny and primate life histories: the case of the giant extinct indroids of Madagascar. In: Plavcan JM, Kay RF, van Schaik CP, Jungers WL, editors. Reconstructing behavior in the primate 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: Kappeler PM, Pereira ME, editors. Primate life histories and socioecology. 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 maternal reproduction and offspring health in rhesus monkeys (Macaca mulatta). Lab Anim Sci 34:66 69. Goss AN. 1984. A comparison of tooth eruption patterns between two colonies of young marmosets (Callithrix jacchus). J Dent Res 63:44 46. Gould L, Sussman RW, Sauther ML. 1999. Natural disasters and primate populations: the effects of a 2-year drought on a naturally 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. Fetal maturity estimation by lecithin/sphingomyelin ratios, pregnancy duration, and caesarian section in chimpanzees. In: Graham CE, Bowen JA, editors. Clinical managment of infant great apes. New York: Alan R. Liss. p 35 42.

Janson C, van Schaik C. 1993. Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA, editors. Juvenile primates: life history, development and behavior. New York: Oxford University Press. p 5776. Jay PC. 1965. The common langur of north India. In: DeVore I, editor. Primate behaviour: eld studies of monkeys and apes. New York: Holt, Rinehart, and Winston. p 197247. Joffe TH. 1997. Social pressures have selected for an extended juvenile period in primates. J Hum Evol 32:593 605. Johnston GW, Dreizen S, Levy BM. 1970. Dental development in the cotton ear marmoset (Callithrix jacchus). Am J Phys Anthropol 33:41 48. Jungers WL. 1988. New estimates of body size in australopithecines. In: Grine FE, editor. Evolutionary history of the robust australopithecines. New York: Aldine de Gruyer. p 115125. Jungers WL. 1997. Orang-utans of the Menage Scientic Expedition to Borneo. Am J Phys Anthropol [Suppl] 24:138 139. Jungers WL, Susman RL. 1984. Body size and skeleton allometry in African apes. In: Susman RL, editor. The pygmy chimpanzee. New York: Plenum Press. p 131177. Jungers WL, Godfrey LR, Simons EL, Wunderlich RE, Richmond BG, Chatrath PS, Rakotosaminanana B. In press. Ecomorphology 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. New York: Kluwer Academic/Plenum Press. Kappeler PM, Ganzhorn JU. 1993. The evolution of primate communities and societies in Madagascar. Evol Anthropol 2:159 171. Kay RF. 1978. Molar structure and diet in extant Cercopithecidae. In: Butler PM, Joysey KA, editors. Development, function and evolution of teeth. London: Academic Press. p 309 339. Keiter MD. 1981. Hand-rearing and development of a lowland gorilla at Woodland Park Zoo, Seattle. Int Zoo Yrbk 21:229 235. Kelley J. 1999. Age at rst molar emergence in Afropithecus turkanensis. 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 167324. Kirkpatrick RC. 1999. Colobine diet and social organization. In: Dolhinow P, Fuentes A, editors. The nonhuman primates. Mountain View, CA: Mayeld Publishing Co. p 93108. Kirkwood JK, Stathatos K. 1992. Biology, rearing, and care of young primates. Oxford: Oxford University Press. Klopfer PH, Boskoff KJ. 1979. Maternal behavior in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 123156. Kozlowski J, Weiner J. 1997. Interspecic allometries are byproducts of body size optimization. Am Nat 149:352380. Kushner H, Kraft-Schveyer N, Angelakos ET, Wudarski EM. 1982. Analysis of reproductive data in a breeding colony of African green monkeys. J Med Primatol 11:77 84. Kuster J. 1983. Longitudinal study of the physical development of hand-reared common marmosets (Callithrix jacchus). In: Seth PK, editor. Perspectives in primate biology. New Delhi: Today & Tomorrow. p 147159. Kuykendall KL, Mahoney CJ, Conroy GC. 1992. Probit and survival analysis of tooth emergence ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes). Am J Phys Anthropol 89:379 399. Lee PC. 1996. The meanings of weaning: Growth, lactation, and life history. Evol Anthropol 5:8796. Lee PC. 1999. Comparative ecology of postnatal growth and weaning among haplorhine primates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. p 111139. Lee PC, Majluf P, Gordon IJ. 1991. Growth, weaning and maternal investment from a comparative perspective. J Zool Lond 225:99 114. Leigh SR. 1994. Ontogenetic correlates of diet in anthropoid primates. Am J Phys Anthropol 94:499 522.
207
Leskes A, Acheson NH. 1971. Social organization of a free-ranging troop of black and white colobus monkeys (Colobus abyssinicus). Proc Int Congr Primatol 3:2231. Lindburg DG. 1977. Feeding behavior and diet of rhesus macaques (Macaca mulatta) in a Siwalik forest in north India. In: Clutton-Brock TH, editor. Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys, and apes. New York: Academic Press. p 223249. MacArthur RH, Wilson EO. 1967. The theory of island biogeography. Princeton: Princeton University Press. Malinow MR, Pope BL, Depaoli JR, Katz S. 1968. Laboratory observations on living howlers. Bibl Primatol 7:224 230. Markham R. 1994. Doing it naturally: reproduction in captive orangutans (Pongo pygmaeus). In: Ogden JJ, Perkins LA, Sheeran L, editors. The neglected ape. San Diego: Zoological Society of San Diego. p 166 170. Markham R, Groves CP. 1990. Brief communication: weights of wild orang utans. Am J Phys Anthropol 81:13. Martin RD. 1983. Human brain evolution in an ecological context. New York: American Museum of Natural History. Martin RD. 1990. Primate origins and evolutiona phylogenetic reconstruction. Princeton: Princeton University Press. Martin RD. 1996. Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:149 156. McKenna JJ. 1982. The evolution of primate societies, reproduction and parenting. In: Fobes JL, King JE, editors. Primate behaviour. London: Academic Press. p 87133. Medway L. 1970. Breeding of silvered leaf monkey, Presbytis cristata, in Malaya. J Mammal 51:630 632. Melnick DJ, Pearl MC. 1987. Cercopithecines in multimale groups: genetic diversity and population structure. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 121134. Meyers DM. 1993. The effects of resource seasonality on behavior and reproduction in the golden-crowned sifaka (Propithecus tattersalli, Simons, 1988) in three Malagasy forests. Ph.D. dissertation, Duke University, Durham, North Carolina. Meyers DM, Wright PC. 1993. Resource tracking: Food availability and Propithecus seasonal reproduction. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum. p 179 192. Middleton CC, Rosal J. 1972. Weights and measurements of normal squirrel monkeys (Saimiri sciureus). Lab Anim Sci 22:583586. Miles P. 1967. Notes on the rearing and development of a handreared spider monkey Ateles geoffroyi. Int Zoo Yrbk 7:82 85. Miller JMA. 1997. A hierarchical analysis of primate brain size and body size: patterns of morphometric variation. Ph.D. dissertation, University of Southern California, Los Angeles, California. Milton K. 1981. Estimates of reproductive parameters for freeranging Ateles geoffroyi. Primates 22:574 579. Mittermeier RA, Tattersall I, Konstant B, Meyers DM, Mast RB, editors. 1994. Lemurs of Madagascar. Washington, DC: Conservation International. Morbeck ME. 1997. Reading life history in teeth, bones, and fossils. In: Morbeck ME, Galloway A, Zihlman A, editors. The evolving 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: British Museum (Natural History). Nash L. 1993. Juveniles in nongregarious primates. In: Pereira ME, 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 howling monkeys, genus Alouatta. In: Mittermeier RA, Rylands AB,
208
L.R. GODFREY ET AL.

Richard AF, Rakotomanga P, Schwartz M. 1993. Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar: 1984 1991. Am J Primatol 30:120. Roberts M. 1994. Growth, development, and parental care in the western tarsier (Tarsius bancanus) in captivity: evidence for a slow life-history and nonmonogamous mating system. Int J Primatol 15:128. Robinson JG, Janson CH. 1987. Capuchins, squirrel monkeys, and atelines: socioecological convergence with Old World Primates. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 69 82. Ross C. 1991. Life history patterns of New World monkeys. Int J Primatol 12:481502. Ross C. 1992. Basal metabolic rate, body weight, and diet in primates: an evaluation of the evidence. Folia Primatol (Basel) 58:723. Ross C, Jones KE. 1999. Socioecology and the evolution of primate reproductive rates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. p 73 110. Rudran R. 1973. The reproductive cycles of two subspecies of purple-faced langurs (Presbytis senex) with relation to environmental factors. Folia Primatol (Basel) 19:41 60. Ru edi D. 1981. Hand-rearing and reintegration of a caesarianborn proboscis monkey Nasalis larvatus at Basle Zoo. Int Zoo Yrbk 21:225229. Rumbaugh DM. 1965. The gibbon infant, Gabrielle: its growth and development. Zoonooz 38:10 15. Rumbaugh DM. 1967. The siamang infant, Sarah: its growth and development. Zoonooz 40:1218. Rumiz DI. 1990. Alouatta caraya: population density and demography in northern Argentina. Am J Primatol 21:279 294. Sauther ML. 1991. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am J Phys Anthropol 84:463 477. Schmid J, Ganzhorn JU. 1996. Resting metabolic rates of Lepilemur rucaudatus. Am J Primatol 38:169 174. Schultz AH. 1941. The relative size of the cranial capacity in primates. Am J Phys Anthropol 28:273287. Schultz AH. 1942. Growth and development of the proboscis monkey. Bull Mus Comp Zool Harvard 89:279 314. Schwartz SM, Kemnitz JW. 1992. Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free ranging rhesus macaques. Am J Phys Anthropol 89:109 121. Siegel MI, Sciulli PW. 1973. Eruption sequences of the deciduous dentition of Papio cynocephalus. J Med Primatol 2:247248. Sirianni JE, Swindler DR. 1985. Growth and development of the pigtailed macaque. Boca Raton, FL: CRC Press. Skinner JD, Smithers RHN. 1990. The mammals of the southern African subregion. Pretoria, South Africa: University of Pretoria. Smith BH. 1989. Dental development as a measure of life history in primates. Evolution 4:683 688. Smith BH. 1992. Life history and the evolution of human maturation. Evol Anthropol 1:134 142. Smith BH, Crummett TL, Brandt KL. 1994. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories. Yrbk Phys Anthropol 37:177231. Smith GE. 1908. On the form of the brain in the extinct lemurs of Madagascar, with some remarks on the the afnities of the Indrisinae. Trans Zool Soc Lond 18:163177. Smith RJ. 1994. Degrees of freedom in interspecic allometry: an adjustment for the effects of phylogenetic constraint. Am J Phys Anthropol 93:95107. Smith RJ. 1999. Statistics of sexual size dimorphism. J Hum Evol 36:423 459. Smith RJ, Jungers WL. 1997. Body mass in comparative primatology. J Hum Evol 32:523559. Smith RJ, Gannon PJ, Smith BH. 1995. Ontogeny of australopithecines and early Homo: evidence from cranial capacity and dental eruption. J Hum Evol 29:155168.
Coimbra-Filho AF, Fonseca GAB, editors. Ecology and behavior of neotropical primates, volume 2. Washington, DC: World Wildlife Fund. p 349 453. Nishida T, Takasaki H, Takahata Y. 1990. Demography and reproductive proles. In: Nishida T, editor. The chimpanzees of the Mahale mountains: sexual and life history strategies. Tokyo: University of Tokyo Press. p 6398. Oates JF, Davies AG, Delson E. 1994. The diversity of living colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behavior, and evolution. Cambridge: Cambridge University Press. p 4573. Ockerse T. 1959. The eruption sequence and eruption times of the teeth of the vervet monkey. J Dent Assoc S Afr 14:422 424. Orgeldinger M. 1994. Monitoring body weight in captive primates, with special reference to siamangs. Int Zoo News 41:17 26. Overdorff DJ. 1993. Similarities, differences, and seasonal patterns in the diets of E. rubriventer and E. fulvus rufus in Ranomafana National Park, Madagascar. Int J Primatol 14: 721752. Overdorff DJ, Strait SG. 1998. Seed handling by three prosimian primates in southeastern Madagacar: implications for seed dispersal. 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 in southeastern Madagascar. Am J Phys Anthropol 108:295310. Pagel M. 1992. A method for the analysis of comparative data. J Theor Biol 156:431 432. Patino E, Borda JT, Ruiz JC. 1996. Sexual maturity and seasonal reproduction in captive Cebus apella. Lab Primate Newslett 35:8 10. Payne J, Francis CM. 1985. A eld guide to mammals of Borneo. Sabah, Malaysia: Sabah Society. Pereira ME. 1993. Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum Press. p 205221. Peres CA. 1994. Which are the largest New World monkeys? J Hum Evol 26:245249. Peters RH. 1983. The ecological implications of body size. Cambridge: Cambridge University Press. Petter J-J, Albignac R, Rumpler Y. 1977. Faune de Madagascar: mammife ` res le muriens (Primates prosimiens). Paris: ORSTOM (CNRS). Petter-Rousseaux A. 1962. Recherches sur la biologie de la reproduction des primates infe rieurs. Mammalia [Suppl] 26:1 88. Pianka ER. 1970. On r- and K-selection. Am Nat 104:592597. Pilbeam D. 1988. Primates. In: Harrison GA, Tanner JM, Pilbeam D, Baker PT, editors. Human biology: an introduction to human evolution, variation, growth, and adaptability, 3rd ed. Oxford: Oxford University Press. p 2771. Pournelle GH. 1967. Observations on reproductive behaviour and early postnatal development of the proboscis monkey (Nasalis larvatus orientalis). Int Zoo Yrbk 7:90 92. Powzyk JA. 1996. A comparison of feeding strategies between the sympatric Indri indri and Propithecus diadema diadema in primary 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 mammals. J Zool Lond 220:417 437. Purvis A, Harvey PH. 1995. Mammal life history evolution: a comparative test of Charnovs model. J Zool Lond 237:259 283. Pusey A. 1990. Behavioral changes at adolescence in chimpanzees. Behaviour 115:203246. Rasamimanana HR, Radinarivo E. 1993. Feeding behavior of Lemur catta females in relation to their physiological state. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. NewYork: Plenum Press. p 123133. Ravosa MJ, Meyers DM, Glander KE. 1993. Relative growth of the limbs and trunk in sifakas: heterochronic, ecological, and functional considerations. Am J Phys Anthropol 92:499 520. Reed DJ, Schwartz GT, Dean C, Chandrasekera MS. 1998. A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes. J Hum Evol 35:427 448.

Snowdon CT, Soini P. 1988. The tamarins, genus Saguinus. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonesca GAB, editors. Ecology and behavior of neotropical primates, volume 2. Washington, DC: World Wildlife Fund. p 223298. Sodaro V. 1993. Hand-rearing and reintroduction of a blackhanded spider monkey Ateles geoffroyi at Brookeld Zoo, Chicago. Int Zoo Yrbk 32:224 228. Sommer V, Srivastava A, Borries C. 1992. Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). Am J Primatol 28:9 27. Stearns SC. 1992. The evolution of life histories. Oxford: Oxford University Press. Stephan H, Frahm H, Baron G. 1981. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol (Basel) 35:129. Strier KB. 1999. The atelines. In: Dolhinow P, Fuentes A, editors. The nonhuman primates. Mountain View, CA: Mayeld Publishing Co. p 109 114. Struhsaker TT. 1975. The red colobus monkey. Chicago: University of Chicago Press. Struhsaker TT, Leland L. 1987. Colobines: infanticide by adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 8397. Sugiyama Y. 1965. Behavioral development and social structure in two troops of Hanuman langurs (Presbytis entellus). Primates 6:381 418. Sussman RW. 1974. Ecological distinctions in sympatric species of Lemur. In: Martin RD, Doyle GA, Walker AC, editors. Prosimian biology. London: Duckworth. p 75108. Sussman RW. 1991. Demography and social organization of freeranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am J Phys Anthropol 84:4358. Sussman RW. 1992. Male life history and intergroup mobility among ringtailed lemurs (Lemur catta). Int J Primatol 13:395 414. Swindler DR. 1976. Dentition of living primates. London: Academic Press. Tan C. 1999a. Group composition, home range size and diet of three sympatric bamboo lemur species (genus Hapalemur) in Ranomafana National Park, Madagascar. Int J Primatol 20: 547566. Tan C. 1999b. Life history and infant rearing strategies of three Hapalemur species. Primate Rep 54:33. Taylor SCS. 1965. A relation between mature weight and time taken to mature in mammals. Anim Product 7:203220. Terranova CJ, Coffman BS. 1997. Body weights of wild and captive lemurs. Zoo Biol 16:1730. Thorington RW Jr, Rudran R, Mack D. 1979. Sexual dimorphism of Alouatta seniculus and observations on capture techniques. In: Eisenberg JG, editor. Vertebrate ecology in the northern neotropics. Washington, DC: Smithsonian Institution Press. p 97106. Tobias PV. 1994. The craniocerebral interface in early hominids. In: Corruccini RS, Ciochon RL, editors. Integrative paths to the past: paleoanthropological advances in honor of F. Clark Howell. Englewood Cliffs, NJ: Prentice Hall. p 185203. Treves A. 1996. A preliminary analysis of the timing of infant exploration in relation to social structure in 17 primate species. Folia Primatol (Basel) 67:152156. Turner TR, Anapol F, Jolly CJ. 1994. Body weights of adult vervet monkeys (Cercopithecus aethiops) at four sites in Kenya. Folia Primatol (Basel) 63:177179.
209
Tutin C. 1994. Reproductive success story: variability among chimpanzees and comparison with gorillas. In: Wrangham RW, McGrew WC, de Waal F, Heltne P, editors. Chimpanzee cultures. Cambridge, MA: Harvard University Press. p 181193. Uehara S, Nishida T. 1987. Body weights of wild chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains National Park, Tanzania. Am J Phys Anthropol 72:315321. Van Horn RN, Eaton GG. 1979. Reproductive physiology and behavior in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p. 79 122. van Roosmalen MGM. 1985. Habitat preferences, diet, feeding strategy, and social organization of the black spider monkey (Ateles paniscus) in Surinam. Acta Amazon [Suppl] 15:1238. Watts DP. 1991. Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211226. Watts DP, Pusey A. 1993. Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks LA, editors. Juvenile primates: life history, development, and behavior. New York: Oxford University Press. p 148 172. Western D. 1979. Size, life history and ecology in mammals. Afr J Ecol 17:185204. Wilen R, Naftolin F. 1978. Pubertal age, weight, and weight gain in the individual female New World Monkey (Cebus albifrons). Primates 19:769 794. Willis MS. 1995. Dental variation in Asian colobines. Ph.D. dissertation, 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 hanuman langurs (Presbytis entellus). Folia Primatol (Basel) 43:123. Winter M 1978. Investigation of the sequence of tooth eruption in hand-reared Callithrix jacchus. In: Rothe H, Wolters H-J, Hearn JP, editors. Biology and behavior of marmosets. Proceedings of the Marmoset Workshop, Go ttingen, September 1977. Go ttingen: Eigenverlag Rothe. p 109 124. Wolfe LG. 1986. Reproductive biology of rhesus and Japanese macaques. Primates 27:95101. Wooldridge FL. 1971. Colobus guereza: birth and infant development in captivity. Animal Behaviour 19:481 485. Wright PC. 1984. Biparental care in Aotus trivirgatus and Callicebus moloch. In: Small MF, editor. Female primates: studies by women primatologists. New York: Liss. p 59 75. Wright PC. 1990. Patterns of parental care in primates. Int J Primatol 11:89 102. Wright PC. 1995. Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar. Int J Primatol 16:835 854. Wright PC. 1997. Behavioral and ecological comparisons of Neotropical and Malagasy primates. In: Kinzey WG, editor. New World primates: ecology, evolution, and behavior. New York: Aldine de Gruyter. p 127141. Wright PC. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yrbk Phys Anthropol 42:3172. Yamashita N. 1998a. Molar morphology and variation in two Malagasy lemur families (Lemuridae and Indriidae). J Hum Evol 35:137162. Yamashita N. 1998b. Functional dental correlates of food properties in ve Malagasy lemur species. Am J Phys Anthropol 106:169 188.
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APPENDIX A APPENDIX A. Life history data, including postcanine dentition at selected ages and life cycle stages (teeth in parentheses may be erupting) Adult mass, (kg) 3.39 ( 3.5 & 3.48 ( 3.62 & 5.94 ( 6.26 & 0.92 ( 1.05 & 3.63 ( 3.52 & 0.748 ( 0.670 & 2.21 ( 2.21 & 2.37 ( 2.51 & 2.18 ( 2.25 & 0.761 ( 0.779 & 0.187 ( 0.173 & 0.362 ( 0.381 & 0.468 ( 0.484 & 0.343 ( 0.358 & 0.779 ( 0.662 & 3.18 ( 2.29 & 3.65 ( 2.52 & 0.813 ( 0.736 & 7.16 ( 5.33 & 6.42 ( 4.33 & 7.78 ( 7.29 & 4.26 ( 2.98 & 5.36 ( 3.59 & 10.61 ( 7.97 & 11.2 ( 6.5 & 24.9 ( 13.6 & 25.1 ( 13.3 & 8.2 ( 5.9 & 15.3 ( 10.9 & 8.0 ( 7.3 & 6.61 ( 5.76 & 7.9 ( 6.26 & 20.39 ( 9.83 ( Adult & cranial capacity (cc) 30.5 29.7 40.0 9.8 31.2 14.6 23.4 24.6 25.6 7.4 3.6 7.7 8.9 8.2 23.2 56.8 63.1 16.1 55.4 47.9 106.4 59.2 62.5 81.3 96.2 145.5 158.9 56.6 98.2 66.9 54.5 60.8 82.8 Postcanine dentition at 4 months
3 4 dp2 dp3 dp4 1 2 M1 (M2 ) 3 4 dp2 dp3 dp4 1 2 M1 (M2 ) 3 4 dp2 dp3 dp4 1 M1 4 P3 P2 P4 1 2 M2 M2 2 3 4 dp2 dp3 dp4
Taxon Propithecus tattersalli Propithecus verreauxi Propithecus diadema Avahi laniger Varecia variegata Hapalemur griseus Lemur catta Eulemur macaco Eulemur fulvus Lepilemur rucaudatus Galago moholi Callithrix jacchus Saguinus nigricollis Saguinus fuscicollis Saimiri sciureus Cebus albifrons Cebus apella Aotus trivirgatus Alouatta palliata Alouatta caraya Ateles geoffroyi Chlorocebus aethiops Macaca fascicularis Macaca mulatta Macaca nemestrina Papio cynocephalus (excluding kindae) Papio anubis Kasi vetulus Semnopithecus entellus Trachypithecus franc oisi Trachypithecus cristata Trachypithecus obscura Nasalis larvatus
Postcanine dentition at 1 year

4 1 P3 P2 P4 M1 2 3 M2 M3 4 1 P3 P2 P4 M1 2 3 M2 M3 4 1 P3 P2 P4 M1 2 3 M2 M3 4 1 P3 P2 P4 M1 2 3 M2 M3 2 3 4 dp2 dp3 dp4 1 2 M1 M2 2 3 4 dp2 dp3 dp4 1 2 4 M1 M2 (P4 ) 2 3 4 dp2 dp3 dp4 1 2 M1 M2 (P4) 2 3 4 dp2 dp3 dp4 1 2 M1 M2 2 3 4 dp2 dp3 dp4 1 2 M1 (M2 ) 2 3 4 P2 P3 P4 1 2 3 M1 M2 M3 2 3 4 P2 P3 P4 1 2 3 M1 M2 M3 2 3 4 P2 P3 P4 1 2 M1 M2 2 3 4 P2 P3 P4 1 2 M1 M2 2 3 4 P2 P3 P4 1 2 M1 M2 2 3 4 dp2 dp3 dp4 1 2 M1 M2 2 3 4 dp2 dp3 dp4 1 (M1 ) 2 3 4 dp2 dp3 dp4
Age at weaning, in years 0.42 0.50 0.50 0.41 0.40 0.33 0.49 0.37 0.50 0.33 0.23 0.21 0.21 0.25 0.50 0.75 1.14 0.49 0.89 0.89 2.25 0.60 1.17 0.88 1.00 1.25 1.6 0.60 1.14 1.08 1.0 1.00 0.77
Postcanine dentition at weaning

4 1 dp2 dp3 P4 M1 2 M2 4 dp2 dp3 dp4 1 2 4 M1 M2 (P4 ) 4 dp2 dp3 dp4 1 2 4 M1 M2 (P4 ) 4 1 P3 P2 P4 M1 2 M2 2 3 4 dp2 dp3 dp4
Age at & rst breeding, in years 4.5 4.57 4.51 2.58 2.72 2.73 2.63 1.66 2.66 1.63 0.71 1.67 2.33 2.33 2.50 4.00 5.78 2.42 3.99 3.71 6.39 4.75 3.90 4.19 3.90 5.50 4.50 4.0 3.90 4.0 4.0 4.0 4.5 (Continued)
dp dp dp
2 2 1 3 3
2 2
3 3
4 4 4 4
dp dp dp
2 2 1 1 2 2 1 3 3
2 2
3 3
4 4 4 4
dp dp dp (M ) 2 3 4 dp2 dp3 dp4

2 3 4 dp2 dp3 dp4
dp dp dp M M (M P ) 3 4 P dp3 P4 2 3 M M2 M3 3 4 dp dp3 dp4 M 3 4 dp dp3 dp4 M 3 4 dp dp3 dp4 dp dp dp

2 3 dp2 dp3 2 2 3 3 4 4
2 2 1 1 4 4 2 2 1 1 2 2 1 1 2 2 1 1 2 2
3 3 2 2
4 4 3 3
dp dp dp M 3 4 dp dp3 dp4 (M ) 2 3 4 dp2 dp3 dp4 1 (M1 ) 2 3 4 dp2 dp3 dp4 1 2 3 4 M1 M2 (M3 P4 )
2 3 4 dp2 dp3 dp4 1 2 3 2 M1 M2 M3 (P2 ) 2 3 4 dp2 dp3 dp4
dp dp dp dp dp dp
2 2 1 1 2 2 3 3 2 2 3 3
2 2
3 3
4 4 4 4 4 4
dp dp dp M 3 4 dp dp3 dp4 dp (M dp M dp M dp (M dp M dp
2 2 1 1 2 2 1 1 2 2 1 1 2 2 1 1 2 2 1 1 3 3 3 3
dp dp
2 2 2 2
2 2
3 3 3 3 3 3 4 4 4 4
dp dp dp dp dp dp
2 3 4 dp2 dp3 dp4
dp dp dp dp dp
3 3 3 3
2 2
3 3 4 4
dp M dp M dp M dp M dp
2 2 1 1 2 2 1 1 2 2 1 1 2 2 1 1 3 3 3 3
P P M M dp dp
3 4 3 4 2 3 2 3 3 4 3 4
dp dp ) 3 4 dp3 dp4 dp dp
3 3 4 4
3 3
4 4
3 4 dp3 dp4 2 M2 3 4 dp3 dp4
dp M
4 4
4 4
1 1
3 4 dp3 dp4 ) 3 4 dp3 dp4 2 M2 4 dp4 4 4
dp dp
dp dp
3 dp3
3 4 dp3 dp4
3 4 dp3 dp4
dp
3 3
dp dp dp dp
3 3
3 3
4 4 4 4
dp dp dp dp
3 3
3 3
4 4 4 4
(dp3) (dp3)
3 4 dp3 dp4
3 4 dp3 dp4 3 4 dp3 dp4 1 (M1 ) 3 4 dp3 dp4 1 (M1 ) 3 4 1 dp3 dp4 M1 2 (M2 ) 3 4 1 dp3 dp4 M1
3 4 dp3 dp4 3 4 dp3 dp4
dp
3 3 3 3 4 4
dp dp
3 4 dp3 dp4
dp (M dp (M dp
3 3 1 1 3 3 2 2 3 3 3 3 1 1 3 3
dp ) 4 1 dp4 M1 ) 4 1 dp4 M1
4 4
4 4
dp
3 3
3 4 dp3 dp4
dp dp (M ) 4 1 dp dp4 M1
3 3 1 1 3 3
4 4
dp dp (M ) 4 dp dp4

APPENDIX A (Continued) Adult mass, (kg) 12.3 ( 8.25 & 13.5 ( 9.2 & 5.90 ( 5.34 & 11.9 ( 10.7 & 78.2 ( 35.7 & 49.6 ( 40.4 & 169.4 ( 80.0 & Adult & cranial capacity (cc) 64.8 69.0 102.2 113.5 374.5 371.1 455.6 Postcanine dentition at 4 months
3 4 dp3 dp4
211
Age at & rst breeding, in years 4.08 4.75 6.69 5.18 14.32 13.90 10.3
Taxon Piliocolobus badius Colobus guereza Hylobates lar Hylobates syndactylus Pongo pygmaeus Pan troglodytes Gorilla gorilla
Postcanine dentition at 1 year

3 4 1 dp3 dp4 M1 2 M2 3 4 1 dp3 dp4 M1 2 (M2 ) 3 4 dp3 dp4
Age at weaning, in years 1.43 1.08 1.50 1.75 5.0 5.0 3.5
Postcanine dentition at weaning

3 4 1 dp3 dp4 M1 2 3 4 M2 (P3 P4 ) 3 4 1 dp3 dp4 M1 2 (M2 ) 3 4 dp3 dp4
dp dp dp dp
3 3 3 3
3 3
4 4
dp dp
3 3
4 4
dp dp M
3 3
4 4
1 1
3 4 dp3 dp4
dp dp dp dp
3 3
3 3
4 4 4 4
3 4 1 dp3 dp4 M1 2 M2 3 4 1 dp3 dp4 M1
dp dp M
3 3
4 4
1 1
APPENDIX B. Sources for life history data, cranial capacities, and dental schedules, with notes Genus and species P. tattersalli Notes Estimates uncertain due to small sample size. Sample includes one immature captive specimen of known age. Dentition at 1 year and age at rst breeding estimated on basis of growth records and comparisons with P. verreauxi and P. diadema. Cranial capacity based on single adult male specimen at American Museum of Natural History. Dental eruption schedule reconstructed using Eaglen (1985), Smith et al. (1994), captive specimens of known age, and immature wildcaught specimens aged on basis of collection date. Mean cranial capacity calculated for pooled sexes. Dental eruption schedule reconstructed using captive and wild specimens of known age, and immature wild-caught specimens aged on basis of collection date. Adult body mass calculated for pooled subspecies. Dental eruption schedule reconstructed using immature wild-caught specimens aged on basis of collection date. Age at female rst breeding estimated using estimates of age at rst emigration from social group and gestation length, assuming reproductive synchrony. Cranial capacity based on pooled sexes. Dental eruption schedule reconstructed using Smith et al. (1994), Eaglen (1985), captive specimens of known age and immature wildcaught specimens aged on basis of collection date. Body mass values based on V. v. variegata. Dental eruption schedule reconstructed using immature wild-caught specimens aged on basis of collection date. Dental eruption schedule reconstructed using data from Eaglen (1985), Smith et al. (1994), captive specimens of known age, and immature wild-caught specimens aged on basis of collection date. Dental eruption schedule reconstructed using Smith et al. (1994), Eaglen (1985), captive specimens of known age, and immature wildcaught specimens aged on basis of collection date. Body mass based on means for the two subspecies, captive individuals. Sources Meyers (1993), Meyers and Wright (1993), Ravosa et al. (1993), and growth records of Duke University Primate Center.
Propithecus verreauxi
Eaglen (1984), Garbutt (1999), Martin (1990), Ravosa et al. (1993), Richard et al. (1993), Roberts (1994), Smith et al. (1994), Stephan et al. (1981), and records of Duke University Primate Center. Glander et al. (1992), Meyers and Wright (1993), Miller (1997), Powzyk (1996), Smith and Jungers (1997), Wright (1995), and personal communication from Claire Hemingway and Patricia Wright. Albignac (1981), Glander et al. (1992), Martin (1990), Petter-Rousseaux (1962), and personal communication from Patricia Wright.
Propithecus diadema
Avahi laniger
Varecia 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), and records of Duke University Primate Center and Parc Tsimbazaza. Garbutt (1999), Tan (1999a,b), Wright (1990), and personal communication from Christina Grassi and Chia Tan. Eaglen (1985), Gould et al. (1999), Hrdlic ka (1925), Klopfer and Boskoff (1979), Mittermeier et al. (1994), Pereira (1993), Rasamimanana and Randinarivo (1993), Smith et al. (1994), Sussman (1991, 1992), and records of Duke University Primate Center and Zurich Zoo. 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.
Hapalemur griseus Lemur catta
Eulemur macaco
(Continued)
212
L.R. GODFREY ET AL.

APPENDIX B (Continued)
Genus and species Eulemur fulvus
Notes Dental eruption schedule reconstructed using Eaglen (1985), Smith et al. (1994), captive specimens of known age, and immature wildcaught specimens aged on basis of collection date. Body mass values based on means for E. f. rufus. Adult female cranial capacity based on Smith (1908) and unpublished data from the United States National Museum. Dental eruption schedule reconstructed using immature wild-caught specimens aged on basis of collection date. Estimate for weaning based on value reported for L. mustelinus. Dental eruption schedule reconstructed using immature wild-caught specimens aged on basis of collection date or mass, and knownaged captive specimens, plus data in Smith et al. (1994) and comparisons to G. senegalensis growth records. Dental eruption schedule from Smith et al. (1994), Swindler (1976), and Winter (1978). Dental eruption schedule from Chase and Cooper (1969) and Smith et al. (1994). Age at female rst breeding estimated on basis of published values for closely related S. fuscicollis. Cranial capacity based on pooled sex data. Dental eruption schedule based on Smith et al. (1994) and Snowdon and Soini (1988). Cranial capacity based on pooled sex data. Data on dental eruption from Galliari and Colillas (1985), Hershkovitz (1977), and Smith et al. (1994). Data on dental eruption from Fleagle and Schafer (1982). Data on dental eruption from Galliari (1985) and Smith et al. (1994)
Sources Eaglen (1985), Eisenberg (1981), Glander et al. (1992), Kappeler and Ganzhorn (1993), Overdorff et al. (1999), Roberts (1994), Smith (1908), Smith et al. (1994), and records of Ivoloina, Duke University Primate Center, and Indianapolis Zoo.
Lepilemur rucaudatus Galago moholi
Bauchot and Stephan (1966), Garbutt (1999), Nash (1993), Peter et al. (1977), Schmid and Ganzhorn (1996), Smith and Jungers (1997). Doyle (1979), Harcourt and Bearder (1989), Izard and Nash (1988), Kirkwood and Strathatos (1992), Nash (1993), Skinner and Smithers (1990), Smith et al. (1994), Van Horn and Eaton (1979). Epple (1970), Goss (1984), Hearn (1982), Johnston et al. (1970), Kuster (1983), Miller (1997), Ross (1991), Smith et al. (1994), Swindler (1976), Winter (1978). Chase and Cooper (1969), Harvey et al. (1987), Hernandez-Camacho and Deer (1985), Hershkovitz (1977), Ross and Jones (1999), Smith et al. (1994), Smith et al. (1995), Snowdon and Soini (1988). Harvey et al. (1987), Ross and Jones (1999), Smith et al. (1994), Smith et al. (1995), Snowdon and Soini (1988). Baldwin and Baldwin (1981), Baldwin (1985), Galliari and Colillas (1985), Hershkovitz (1977), Kinzey (1997), Middleton and Rosal (1972), Miller (1997), Smith et al. (1994). Fleagle and Schafer (1982), Hernandez-Camacho and Deer (1985), Miller (1997), Ross (1991), Smith and Jungers (1997), Wilen and Naftolin (1978). Ayers (1986), Eisenberg (1989), Fleagle and Mittermeier (1980), Fragaszy and Adams-Curtis (1997), Fragaszy and Bard (1997), Galliari (1985), HernandezCamacho and Deer (1985), Miller (1997), Patino et al. (1996), Robinson and Janson (1987), Ross (1991); Smith and Jungers (1997). Hall et al. (1979), Kinzey (1997), Miller (1997), Ross (1991), Smith and Jungers (1997), Wright (1984, 1997). 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). Malinow et al. (1968), Miller (1997), Neville et al. (1988), Ross and Jones (1999), Rumiz (1990), and records of Cheyenne Mountain Zoological Park and Audobon Park and Zoological Gardens. Carpenter (1935), Chapman (1987), Eisenberg (1981), Fedigan and Rose (1995), Glander et al. (1991), Miles (1967), Miller (1997), Milton (1981), Robinson and Janson (1987), Schultz (1941), Smith et al. (1994), Sodaro (1993), Strier (1999), van Roosmalen (1985), and records of Pittsburgh Zoo. Butynski (1988), Kushner et al. (1982), Melnick and Pearl (1987), Miller (1997), Ockerse (1995), Ross (1991), Smith et al. (1994), Turner et al. (1994). Fooden (1995), Harvey et al. (1987), Iwamoto et al. (1984), Miller (1997), Ross (1991), Smith et al. (1994). (Continued)
Callithrix jacchus Saguinus nigricollis
S. fuscicollis Saimiri sciureus
Cebus albifrons Cebus apella
Aotus trivirgatus
Alouatta palliata
Data on dental eruption are from Hall et al. (1979). Data on weaning are taken from records compiled at Woodland Park Zoological Gardens. Dental eruption schedule inferred from data presented by Froehlich et al. (1981), Glander (1980), and Neville et al. (1988). Dental eruption schedule inferred from data presented by Malinow et al. (1968) and Neville et al. (1988). Dental eruption schedule inferred on basis of published comparisons with Cebus as well as a few records for Ateles geoffroyi (Carpenter, 1935; Miles, 1967; Smith et al., 1994; Sodaro, 1993). Dentition at weaning estimated on basis of eruption schedule for Cebus coupled with late age at weaning in Ateles. Dental eruption schedule from Smith et al. (1994) and Ockerse (1959) Dental eruption schedule from Smith et al. (1994) and Iwamoto et al. (1984).
A. caraya
Ateles geoffroyi
Chlorocebus aethiops Macaca fascicularis

APPENDIX B (Continued) Genus and species M. mulatta Notes Dental eruption schedule from Smith et al. (1994) and Hurme and van Wagenen (1953). Sources
213
M. nemestrina Papio cynocephalus Papio anubis Kasi vetulus Semnopithecus entellus
Dental eruption schedule from Smith et al. (1994) and Sirianni and Swindler (1985). Dental eruption schedule from Smith et al. (1994) and Siegel and Sciulli (1973). Dental eruption schedule from Smith et al. (1994). Dental schedule reconstructed using data on body mass, coat color, Hill (1937), Leighs (1994) growth curves, and Smith et al. (1994). Dental schedule reconstructed using data on body mass, coat color (Sugiyama, 1965; Jay, 1965; Winkler et al., 1984), Leighs (1994) growth curves, and known-aged captive individuals from collections of San Diego State University and California Primate Research Center at Davis. Dental schedule uncertain due to small available sample of skulls. Known-aged individuals housed at San Diego State University establish accelerated dental eruption schedule. Cranial capacity estimated using regression analysis of adult & cranial volume on adult & skull size for colobines only. Age at weaning and rst breeding were estimated on basis of review by BrandonJones (1985). Dental schedule reconstructed using data on body mass, coat color (Bernstein, 1968; Payne and Francis, 1985), and Leighs (1994) growth curves. Dental schedules were reconstructed using data on body mass, coat color, Leighs (1994) growth curves, one known-aged individual from Anthropological Institute and Museum in Zurich, and observations by Horwich (1974). Age at weaning and female rst breeding estimated on basis of review by Brandon-Jones (1985). Dental schedule reconstructed using data on body mass, coat color (Brandon-Jones, 1985; Payne and Francis, 1985), and Ru edi (1981) growth curves. On the basis of an observation by Schultz (1942) that actually pertains to macaques, Napier (1985) incorrectly reports full eruption of the permanent dentition at 7 years. Schultz (1942) actually states that dental eruption in female proboscis monkeys is complete prior to sexual maturation. Dental schedule reconstructed using data on body mass (Natural History Museum, London), coat color (Crandall, 1964; Horwich and Manski, 1975; Leskes and Acheson, 1971; Wooldridge, 1971), and Leighs (1994) growth curves. Dental schedule reconstructed using data on body mass, coat color (Struhsaker, 1975), and Leighs (1994) growth curves. Body mass data for P. b. oustaleti. Dental eruption schedule from Ibscher (1967), Rumbaugh (1965, 1967), and Smith et al. (1994).
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). Fooden (1975), Harvey et al. (1987), Miller (1997), Ross (1991), Sirianni and Swindler (1985). Bentley-Condit and Smith (1997), Lee (1999), Miller (1997), Napier (1981), Ross (1991), Siegel and Sciulli (1973), 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). 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). Hrdy (1980), Jay (1965), Leigh (1994), Miller (1997), Napier (1985), Sommer et al. (1992), Struhsaker and Leland (1987), Sugiyama (1965), Willis (1995), Winkler et al. (1984).
Trachypithecus franc oisi
Gibson and Chu (1992), Willis (1995), and records of San Diego State University.
Trachypithecus cristata
Bernstein (1968), Brandon-Jones (1985), Leigh (1994), Medway (1970), Miller (1997), Payne and Francis (1985), Willis (1995), and personal communication from Jacqui Browman. Brandon-Jones (1985), Curtin and Chivers (1978), Horwich (1974), Leigh (1994), Miller (1997), Smith and Jungers (1997).
Trachypithecus obscura
Nasalis larvatus
Brandon-Jones (1985), Hollihn (1973), Kirkwood and Stathatos (1992), Miller (1997), Payne and Francis (1985), Pournelle (1967), Ross (1992), Ru edi (1981), Schultz (1942), Smith and Jungers (1997).
Colobus guereza
Crandall (1964), Harvey et al. (1987), Horwich and Manski (1975), Leigh (1994), Leskes and Acheson (1971), Miller (1997), Oates et al. (1994), Ross and Jones (1999), Smith and Jungers (1997), Wooldridge (1971), and records of Colombus Zoological Gardens. Leigh (1994), Miller (1997), Oates et al. (1994), Ross and Jones (1999), Smith and Jungers (1997), Struhsaker (1975). 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 of Indianapolis Zoo. (Continued)
Piliocolobus badius
Hylobates lar
214
L.R. GODFREY ET AL.

APPENDIX B (Continued)
Genus and species H. syndactylus Pongo pygmaeus
Notes Dental eruption schedule from Rumbaugh (1967) and Smith et al. (1994) Dental eruption schedule from Smith et al. (1994) and Fooden and Izor (1983) supplemented by zoo records. Dental eruption schedule from Anemone et al. (1996), Conroy and Mahoney (1991), Fleagle (1998), Kuykendall et al. (1992), and Smith et al. (1994). Adult body masses are equally weighted pooled subspecies values. Dental eruption schedule from Smith et al. (1994), Keiter (1981), and Willoughby (1978). Adult body masses are equally weighted pooled subspecies values.
Sources Fox (1984), Geissmann (1991), Miller (1997), Orgeldinger (1994), Rumbaugh (1967), Smith et al. (1994). Fooden and Izor (1983), Galdikas (1985), Jungers (1988, 1997), Markham and Groves (1990), Markham (1994), Smith et al. (1994), Tobias (1994), Watts and Pusey (1993), and records of Lowry Park Zoological Gardens and Auckland Zoological Park. Anemone et al. (1996), Conroy and Mahoney (1991), Fleagle (1998), Goodall (1986), Graham et al. (1985), Hardin et al. (1975), Kuykendall et al. (1992), Nishida et al. (1990), Pilbeam (1988), Pusey (1990), Ross (1991), Smith et al. (1994), Smith and Jungers (1997), Tobias (1994), Tutin (1994), Uehara and Nishida (1987); Watts and Pusey (1993). 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).
Pan troglodytes
Gorilla gorilla

Teeth, Brains, and Primate Life Histories

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 114:192214 (2001)

Teeth, Brains, and Primate Life Histories

2001 Wiley-Liss, Inc.

2001 WILEY-LISS, INC.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

Lepilemuridae Galagonidae Callitrichidae Cebidae

Hylobatidae Pongidae Hominidae

L.R. GODFREY ET AL.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

L.R. GODFREY ET AL.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

L.R. GODFREY ET AL.

The protein richness hypothesis (PRH)

DCH, design constraint hypothesis; BPH, brain pleiotropy hypothesis.

Test of null hypothesis with P values

No 0.997 (0.903) 40 (11) 0.43

Log cranial capacity Log cranial capacity

Predictions of working hypothesis

Dental precocity at 4 months Dental precocity at 1 year Dental precocity at weaning

Log cranial capacity Log cranial capacity Log cranial capacity

Log adult & mass Log adult & mass

Explanatory variable Controlled variable Partial r N (N eff.)

Folivores exhibit faster dental development than do like-sized frugivores.

Diet: vs. Diet: vs. Diet: vs.

frugivores folivores frugivores folivores frugivores folivores

Yes, cannot reject null hypothesis

L.R. GODFREY ET AL.

No 0.195 (0.365) 0.14 40 (9)

Test of null hypothesis with P values

TABLE 6. Test of the risk aversion hypothesis (unique predictions in bold)

Dental precocity at 4 months Dental precocity at 1 year Age at weaning

Folivores exhibit faster dental development than do like-sized frugivores.

Predictions of working hypothesis

Age at rst breeding Dental precocity at 4 months Dental precocity at 1 year

TABLE 7. Test of food processing hypothesis (unique predictions in bold)

Dependent variable Partial r N (N eff.)

Folivores exhibit faster dental development than do like-sized frugivores.

L.R. GODFREY ET AL.

Folivores exhibit faster dental development than do like-sized frugivores.

Predictions of working hypothesis

Test of null hypothesis with P values

0.552 (0.521) 0.03 22 (6)

TABLE 8. Test of protein richness hypothesis (unique predictions in bold)

Dental precocity at 4 months Dental precocity at 1 year Age at weaning

Age at rst breeding Dental precocity at 4 months Dental precocity at 1 year

Age at rst breeding Age at weaning

L.R. GODFREY ET AL.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

L.R. GODFREY ET AL.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

L.R. GODFREY ET AL.

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES

L.R. GODFREY ET AL.

Postcanine dentition at 1 year

Postcanine dentition at weaning

dp dp dp (M ) 2 3 4 dp2 dp3 dp4

dp dp dp M M (M P ) 3 4 P dp3 P4 2 3 M M2 M3 3 4 dp dp3 dp4 M 3 4 dp dp3 dp4 M 3 4 dp dp3 dp4 dp dp dp

2 3 4 dp2 dp3 dp4

3 4 dp3 dp4 2 M2 3 4 dp3 dp4

3 4 dp3 dp4 ) 3 4 dp3 dp4 2 M2 4 dp4 4 4

3 4 dp3 dp4 3 4 dp3 dp4

TEETH, BRAINS, AND PRIMATE LIFE HISTORIES