AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 66:307-315 (1985) Behavioral Correlates of Tooth Eruption in Madagascar Lemurs ROBERT H. EAGLEN Department of Anatomy, University of Puerto Rico, Medical Sciences Campus, Sun Juan, Puerto Rico 00936 KEY WORDS Dental eruption, Lemurs, Feeding behavior, Growth ABSTRACT Observations on the sequence and timing of gingival tooth eruption are reported for six species of Madagascar lemurs. Complete sequences of eruption were obtained for the deciduous dentition, and partial to complete sequences were recorded for the permanent dentition. In CheirogaZeus medius and in four species of the genus Lemur, the deciduous teeth erupt in front-to-back sequence, with the toothcomb emerging near birth as an integrated complex. In Propithecus verreauxi the same pattern is exhibited, but the small peglike lower canine and dp3 erupt last. Eruption of the permanent dentition in Lemur species takes place in two distinct stages. In the first stage the upper incisors, toothcomb, and first two molars penetrate the gingiva. After a n interval of 3 to 4 months, the remaining permanent teeth erupt. Deciduous premolars erupt when young animals are being weaned. The eruption of the deciduous toothcomb appears unrelated to feeding or grooming behavior. In L. catta and L.fulvus, the first stage of permanent tooth eruption occurs at approximately 6 months of age, when the growth rate slows down and (in wild populations) the rainy season is ending. This suggests that eruption of the anterior molars is timed to coincide with a shift from a more frugivorous to a more folivorous dietary regime, which occurs during the dry season. No further tooth eruption occurs until approximately 1 year of age, when the growth rate increases and the rainy season returns for wild populations. Thus, the second wave of permanent tooth eruption in these species again appears linked to changing climatic conditions which lead to a shift in dietary preferences. Previous studies of dental eruption among MATERIALS AND METHODS nonhuman primates have tended to focus on Most of the data reported here were obone of two aspects of the data. Some studies tained by physical examination of the oral (e.g., della Serra, 1952; Schwartz, 1974) have cavities of live animals. From February 1977 concentrated on the phylogenetic implica- through August 1978, using the resources of tions of dental eruption sequences, while the Duke University Center for the Study of others (e.g., Tappen and Severson, 1971; Re- Primate Biology and History, I examined the lethford et al., 1982; Glassman, 1983) have dentitions of growing lemurs (Table 1). Leemphasized the use of dental eruption se- mur and Propithecus subjects were examined quences and eruption timing for the estima- once every 2 weeks; Cheirogaleus subjects tion of chronological age. In this report I were examined twice each week. During each present data on the sequence and timing of examination, the subject was weighed. The dental eruption among some Madagascar le- relative states of eruption of individual teeth murs, with a rather different emphasis; my were estimated by visual inspection of the primary purpose is to relate certain aspects Received November 28, 1983; revised February 27, 1984; acof Iemuroid dental eruption to emerging and cepted March 8,1984. mature behavioral patterns. Duke University Primate Center Publication No. 264. 0 1985 ALAN R. LISS, INC. 308 R.H. EAGLEN duous dentition of each species used in this study. As those sequences indicate, there is a reasonably homogeneous pattern within each jaw as to the sequence in which lemur teeth erupt. For all species of the genus Lemur described in this study, the mandibular deciduous dentition erupts in a front-to-back sequence, with the toothcomb emerging as a functional unit. The premolar eruption sequence indicated here is identical to the alveolar eruption sequences described by Schwartz (1974) for the same species. A similar pattern occurs in Cheirogaleus medius. The only difference between this species and the genus Lemur is that the posterior deciduous premolar appeared to be more completely erupted than the middle premolar a t the time these teeth were first seen. Schwartz (1974) inferred a 2-4-3 sequence of deciduous premolar eruption for C. medius. While his sequence is different than that reported here and may indeed be technically correct, I should also note that the middle and posterior premolars made their first appearance simultaneously, and the difference in their respective crown heights was RESULTS not particularly striking. From a functional Deciduous eruption sequences point of view, tbe contradiction in the two Table 3 summarized the inferred sequence eruption sequences is not likely to have any and timing of gingival eruption for the deci- great significance. oral cavity, sometimes with the aid of a Beebe magnifying binocular loupe. After weighing and oral examination, each subject was returned to its social group. A simple scoring system was used to estimate the degree of dental eruption. A tooth was scored as 0 (newly erupted) when it first appeared to penetrate the surrounding gingival tissue. It was scored as 1in subsequent inspections if the complete crown surface was visible above the gingival plane, but the tooth was lower in crown height than adjacent teeth of equivalent size. A tooth was scored as 2 (fully erupted) if the complete crown surface was visible and it either exceeded the height of adjacent teeth scored as 1, or equaled the height of adjacent teeth scored as 2. Additional observations on the eruption of the deciduous dentition were obtained by examining the oral cavities of deceased infants and juveniles, and by fortuitous examination of some live animals removed from their social groups for weighing and permanent identification marking (Table 2). TABLE I . Subjects used i n contmuine xtudv Species Lemur catta L. fuluus L. macaw L. uariegatus Propithecus uerreauxi Cheirogaleus medius 'Twins. 'Triplets. ID No. Sex Study dates_- 2583 3547 3592 2586 2589 3556 3585 3504 3548l 3549l 3555 3509 3514 3557l 3558' 3580' 3581' 3582' 1593 632 633 F M F F F M M F M M M F M F M F F M M F M 3122177-8131178 4127178-8125178 6112178-8125178 4107177-8/31/78 4107177-8131178 4114178-813 1178 5130178-8131178 412 1177-8131178 4110178-8114178 4110178-8/14/78 4114178-8131178 5119177-8131178 5119177-8/31/78 4114178-8125178 4114178-8125178 6102178-8125178 6102178-8/25/78 6102178-8125178 2115177-7114177 6129178-8131178 6126178-8131178 Age span during study (days) 10-509 31-151 25-99 20 -531 21-532 11-150 24-117 27-524 11-137 11-137 13-152 30-499 28-497 10-143 10-143 29-113 29-113 29-113 9-158 10-73 7-73 309 TOOTH ERUPTION IN LEMURS TABLE 2. Subjects examined fortuitously ID No. Species Sex Date examined ~ Lemur catta L. fulvus L. uariegatus 2502' 35442 35452 1553' 2546' 2570' 3567 3542 3541 3539 1557' 1560' 1574' 2562' 2564' 3573 M F F F M F 623' 636 627 M M Cheirogaleus medius F F F M F M M F M M 2/11/77 4/14/78 4/14/78 2/11/77 2111177 2/11/77 5/10/78 4/14/78 4114178 4/14/78 2/11/77 2/11/77 2/11/77 2/11/77 211 1/77 6/12/78 6/22/78 2/11/77 6/26/78 7/07/77 7/14/77 Age when examined (days) 1 18 18 21 1 13 22 24 25 26 36 86 133 0 46 50 60 2 7 9 16 'Cadaver. 'Twins. TABLE 3. Sequence and timing of deciduous tooth eruption' Species Lemur catta L fuluus L. macaco Week 1 Week2 Latest age of gingival eruption (end of each respective week) Week3 Week4 Week6 Week8 Week 10 tc C tc ? ? L. uuriegatus c-5 Propithecus uerreauxi Cheiroguleus medius (C,P4) 0 C (P2,P3.P4) O G a - (il,i2) 'tc, deciduous toothcomb; lower "canine" of J? uerreauxi is the equivalent of dp, recognized by Schwartz (1974). Teeth grouped in parentheses emerged "simultaneously,"i.e., on day of observation; sequencing within parenthetical groups inferred from differences in crown height at time of first observation. Propithecus verreauxi also shows a mesiodistal sequence of eruption for the mandibular deciduous dentition, but only for those teeth which serve as functional units in occlusion. The rudimentary, peglike lower canine and dps erupt at a later date than the remaining mandibular teeth. Since the former teeth are quite small, it is quite possible that alveolar eruption sequences may differ from gingival eruption sequences. A slightly different but relatively consistent pattern characterizes the eruption sequence of the maxillary deciduous dentition. For most species described here, the upper deciduous canine is the first maxillary tooth to erupt, followed in sequence by the anterior, middle, and posterior premolars. In most cases, the lateral upper incisor is next to erupt, followed by the central upper incisor; in L. fulvus and €? verreauxi, however, one or 310 R.H. EAGLEN both of the deciduous upper incisors may penetrate the gingiva before all premolars have begun their eruption. The lateral upper incisor was always seen before the central upper incisor, but incisors a s a group were variable both within and between species in terms of their timing of eruption relative to the premolar complement. The difference in the sequence of incisor eruption between upper and lower jaws could well be a reflection of the diminutive size of upper incisors among lemurs, and again it would not be surprising if other investigators reported contradictory sequences on the basis of alveolar eruption. With few exceptions, any given mandibular deciduous tooth erupts earlier than its maxillary counterpart. A similar phenomenon has been documented in the deciduous eruption sequences of Saguinus fuscicollis (Glassman, 1983) and S. nigricollis (Chase and Cooper, 1969). Those studies also note a mesiodistal progression in the sequence of eruption of deciduous teeth, similar to the pattern inferred for the lemur species described here. Table 3 also gives the ages at which teeth erupt. The ages reported are for initial eruption (i.e., the latest age a t which a tooth initially penetrates the gingival tissue). While it might be more interesting to use the age a t which a tooth were fully erupted, and hence formed part of a functioning occlusal unit, I have not reported the data that way because my criterion for complete eruption is somewhat arbitrary, while the criterion for initial eruption is not. Latest ages are reported rather than arithmetical means because of the small sample sizes involved. Among live animal subjects, the deciduous toothcomb invariably began eruption by the middle of the second week. Examination of stillborns indicates that, in fact, the deciduous toothcomb erupts by the time of birth. Among the tamarins described by Chase and Cooper (1969) and Glassman (19831, the incisors and canine were present at birth in both upper and lower jaws. The upper deciduous canine makes its first appearance in all species by the end of the second week. In C. medius, a small (250 gm), rapidly maturing species, most of the deciduous dentition has erupted by this time, the only exceptions being the upper incisors. A similarly rapid pace of deciduous eruption occurs in l? uerreauxi, where the only teeth not to have appeared by the end of the second week are the small central incisor of the up- per jaw, and the rudimentary lower canine and dp3 of the lower jaw. The rapid rate of deciduous eruption in C. medius is perfectly understandable given its small size. The comparable rate of deciduous eruption in l? verreauxi, by contrast, is quite surprising-it is among the largest of the extant Madagascar lemurs. A possible explanation for the fast pace of deciduous tooth eruption in the latter species is afforded by Richard’s (1976) observation of food tasting in a 2-week-oldwild sifaka. If food tasting or mastication were characteristic of the species at this age, it would provide a convincing reason for the rapid eruption of its deciduous teeth. Unfortunately, we don’t know if Richard’s finding is indeed accurate for l? uerreauxi or not; all that can be said is that early ingestion of solid foods has not been reported in other studies of sifakas, either in the wild or in captivity (Eaglen and Boskoff, 1978). Within the genus Lemur, L. catta shows a more precocious eruption of the deciduous dentition than do the remaining species. The deciduous teeth in L. catta have all begun eruption by the middle of the second month; in the other species eruption of deciduous teeth continues into the middle of the third month. The more rapid rate of deciduous tooth eruption in L. catta compared to other Lemur species parallels the generally more rapid behavioral development and earlier independence of the former species (Klopfer and Klopfer, 1970; Sussman, 1977). Permanent eruption sequences The sequence and timing of eruption of the permanent dentition is indicated in Table 4. Sample sizes for these data are much smaller, as they are based only on the subjects born during the first year of the study. Eruption sequences for L. macaco, l? uerreaui, and C. medius are incomplete because the subjects were not available for the full term of the study. The sequences of permanent tooth eruption, like those of the deciduous dentition, manifest certain broad patterns across species. For all six species studied, the anterior permanent molars of each jaw were the first adult teeth to erupt. This event occurred earliest (1%months) in the smallest species, C. medius, and from 4 to 6 months of age in the remaining species. As before, I? uerreauxi and L. catta erupted M1 at a n earlier age than did the other Lemur species. "OOTH ERUPTION IN LEMURS hli 311 In most Lemur species and in C. medius, the toothcomb erupted next as a functional unit, followed by the upper incisors and second molars; the only exception to this pattern was exhibited by L catta, in which the second molars erupted before the appearance of the anterior dentition. By the end of the tenth month, the anterior teeth and first two molars had penetrated the gingiva in all Lemur species. This first wave of permanent tooth eruption was followed by a period of stasis in the genus Lemur. The lag between the eruption of the anterior teeth and first two molars and the appearance of the remaining permanent teeth ranged from 3 to 4 months. By the end of the twelfth month in L. catta, and the end of the thirteenth month in other Lemur species, eruption of the permanent premolars had begun. The sequence of premolar eruption observed in these animals was the same as that reported by Schwartz (1974): 4-3-2 for L. catta, and 2-4-3 for the other species. As Table 4 indicates, the timing of eruption for the posterior molars and the upper canine was somewhat variable between species. Schwartz (1974) noted both interspecific and intraspecific variation in the sequence of initial eruption for these teeth; no intraspecific variation was recorded in this study, but sample sizes were quite small. The emergence of premolars, M3, and the upper canine, while not as distinctly patterned as the eruption of the other permanent teeth, nevertheless occurred fairly rapidly over a period of 3 to 4 months. By 17 months of age, the complete adult dentition had penetrated the gingiva in all of the Lemur species for which data were available. The sequence and timing of eruption of the permanent dentition is similar in some ways to the eruption of the deciduous dentition. In most cases, a given mandibular tooth erupts simultaneously with or earlier than its maxillary counterpart. Eruption of the permanent teeth progresses most rapidly in the smallest species, C. medius. Within the genus Lemur, the most rapid eruption of the permanent dentition takes place in L. catta. The early eruption of M1 in P. verreauxi suggests that this species, like L. catta, also undergoes rapid tooth eruption compared to other Madagascar lemurs of comparable size (e.g., L uariegutus). The pattern of eruption in Lemur is consistent, with teeth emerging in two distinct stages. In the earlier stage, 2 to 3 months 312 R.H.EAGLEN after the deciduous dentition has fully emerged, the toothcomb, upper incisors, and first two molars make their appearance. After a n interval of 3 months or so, the remaining teeth appear in fairly rapid order, and are in place by the middle of the second year. DISCUSSION The data reported here manifest some correlations with the development of certain aspects of feeding behavior. Among species of the genus Lemur, the deciduous premolars erupt during the second month of life; Klopfer and Klopfer (1970) observed that captive L. catta began tasting solid foods a t the end of the first month and were ingesting them by the end of the second month, with L. fulvus and L. variegatus exhibiting a similar pattern. The period during which solid food ingestion is initiated and the deciduous premolars erupt is also a time of constant weight gain for captive Lemur species (Fig. 1). Once the deciduous premolars have erupted and growing animals begin displaying a n interest in solid foods, the process of weaning is initiated. In both captive Lemur species (Klopfer and Klopfer, 1970) and their wild counterparts (Sussman, 19771, weaning begins during the middle of the third month of life. By the middle of the fourth month, young L. catta are largely independent of their mothers, and independence is achieved by young L.. fulvus by the end of the fourth month. In terms of tooth eruption, this period of weaning and behavioral independence is a static one-the only teeth which penetrate the gingiva during this period are the deciduous upper incisors. Weight gain also increases with no discernible change during this period (Fig. l), suggesting that the deciduous premolars are suffkiently efficient during mastication to permit the smooth transition from a suckling mode of feeding to a primarily chewing regime. Eruption of the deciduous premolars may or may not be associated with the transition from maternal milk to solid food in I? verreauxi. In this species the deciduous premolars have erupted by the middle of the first month. As noted earlier, Richard (1976) saw food tasting in a wild sifaka a t that age. Among captive sifakas, however, solid food tasting has not been observed until the middle or late part of the second month (PetterRousseaux, 1962; Albignac, 1969; Eaglen and Boskoff, 1978). One should also note that the timing of premolar eruption reported here is based on a single animal. Thus, the coincidence of deciduous premolar eruption and the onset of solid food experimentation needs further documentation to confirm the hypothesis that the two are related in I! uerreauxi. The emergence of the deciduous toothcomb a t or near the time of birth probably has no behavioral significance. While the permanent toothcomb is used both in feeding and in grooming, neither of these kinds of behavior is manifested by newborn lemurs (except, of course, suckling). Masticatory activity, as noted above, does not as a rule begin before the second month of life; this is probably also true for grooming behavior. Although the literature on lemur behavior seldom discusses the development of grooming, the scant available evidence suggests that it does not begin during the early postnatal period. Klopfer and Dugard (1976)first observed selfgrooming in 1,. variegatus during the second week and a n infant grooming another animal in the fourth week. Eaglen and Boskoff (1978) did not observe self-grooming in I! verreauxi until the fourth week of life. Since the corresponding teeth also appear perinatally in Saguinus fiiscicollis (Glassman, 1983) and S. nigricollis (Chase and Cooper, 1969), it seems unlikely that the perinatal eruption of the deciduous toothcomb among lemurs is in any way related to the unique functions which that structure serves among adults. Little attent.ion has been paid to changes in feeding behavior after the weaning period in lemurs; thus, it is impossible to correlate aspects of permanent tooth eruption directly with corresponding behavioral events. On the other hand, the pattern of tooth eruption in some Lemur species does appear to be linked with changes in growth rate and resource utilization which accompany transitions from wet to dry seasons and vice versa. During the first 6 months of life, growth rates are more or less constant for the Lemur species used in this study (Fig. 1). For the smaller species (L. catta, L. fulvus, L. macaco), born mainly in the months of September and October in Madagascar, the age at which the growth rate slows down (among captive animals) falls near the end of the rainy season, in the months of March and April (Martin, 1972). The change in climate is accompanied by a shift in resource utilization among L. catta and L. fulvus, marked by greater intake of herbaceous plant parts and 313 TOOTH ERUPTION IN LEMURS ,. 2700- variegatus "\ L. c a t t a / - ' I 2400- ,---L. ,/ 2100- L . rnacaco / / ,=-/ ,-*' L . tulvus 18001 E 2 + I 2 w _-' I ,I= 1500- I' " / I ,,;I , - ;- - /=-," L _ , I 1200- 3 900- 600- 300- 8 ,~~ ,', , 16 1 24 32 1.' 1II " , 40 48 I 56 1 64 1 72 1 80 AGE(weeks) Fig. 1. Growth rate of captive L e m w during the first year and a half of life, based on recorded weights of subjects studied over full term of project. Dashed lines along each curve represent the following periods of tooth eruption, respectively: (1) eruption of deciduous premo- lars; (2) stage 1 of permanent tooth eruption (see text for details); (3) stage 2 of permanent tooth eruption. Arrow along age scale indicates ages of captive L. catta and L. fuuluus which correspond to dry season for the wild counterparts of those species. reduction in the intake of fruit (Sussman, 1974). The first phase of permanent tooth eruption, in which the anterior molars and anterior dentitions emerge, spans this transitional period in L. catta and L. fuluus, and extends into the first half of the dry season. Thus, the timing of the first phase of permanent tooth eruption, when placed in the context of changing ecological events which occur during that period among wild Lemur populations, suggests that the two large anterior molars emerge at a time when they can most effectively be used to process fibrous foods. The two permanent molars, together with the deciduous premolars, then serve as the primary battery of masticatory teeth for the remainder of the dry season, when no further permanent tooth eruption takes place. The hypothesis linking the eruption of the anterior molars to increased folivory in the two Lemur species might also apply to P. uerreauxi, whose diet is almost exclusively folivorous. In €? verreauxi the anterior permanent molar erupts a t 4 months of age; in the roughly equal-sized L. variegatus, eruption of the first molar does not occur until 6 months of age. The relatively precocious eruption of M1 in €? verreauxi compared to L uariegatus can then be interpreted as a consequence of the former species' primary dependence on leaves as food after the wean- 314 R.H. EAGLEN ing period ends. The age at which sifakas effect the switch from maternal milk to a leafy diet is not known in the wild, but locomotor independence probably does occur at about 4 months of age (Eaglen and Boskoff, 1978). Assuming that independent feeding is contemporaneous with independent locomotion, the anterior molar of sifakas would appear precisely when needed for mastication. Whether the foregoing analysis applies to other lemurs which are seasonally or always folivorous is unknown. By the same token, little can be said at this time about the behavioral significance of the timing of permanent tooth eruption in species like L. variegatus, where little is known of its behavior in the wild. The second phase of permanent tooth eruption in L. catta, involving the permanent premolars, upper canine, and small posterior molar, occurs a t about 1 year of age. This wave of tooth eruption is accompanied by a n increase in the growth rate (Fig. 1) and corresponds with another period of climatic change, as the dry season gives way to the next rainy season. Thus, temporary disruptions of the continuity of the masticatory tooth row (shedding of deciduous premolars and their replacement by permanent teeth) occur as the diet of L. catta is shifting from tough leaves to more soft fruit. A similar phenomenon occurs among L. fuluus. In general, then, the timing of permanent tooth eruption looks to be keyed to changing patterns of resource availability and resource exploitation in L. catta and L. fuluus. The similar pattern of tooth eruption and weight gain evinced by L. macaco suggests the same hypothesis for that species, although corroborating behavioral data are presently lacking. There is one other aspect of permanent tooth eruption which may have behavioral or functional significance-the sequence in which the permanent premolars erupt. Schwartz (1975) argued that the sequence of permanent premolar eruption in Madagascar lemurs provides a useful feature for lemuroid phylogeny reconstruction. Specifically, he considered the 4-3-2 sequence of permanent premolar eruption in Hapalemur, Lepilemur, and some adapids as evidence for close phylogenetic kinship among those taxa; under this interpretation, the 4-3-2 sequence exhibited by Lemur catta represents a parallelism. An alternative or concomitant functional explanation may be equally viable. Every Madagascar lemur species which is primarily folivorous erupts the posterior permanent premolar before the anterior premolads); this assertion holds true for Hapalemur, Lepile mur, and all extant indriids. Thus, there appears to be a strong correlation between the sequence of permanent premolar eruption and the preferred diet of Madagascar lemurs. Although Lemur catta is not exclusively folivorous, it does consume large quantities of leaves during the dry season (Sussman, 1974), and its molar morphology is in many ways comparable to that of more folivorous species (Kay et al., 1978). This would appear to enhance the notion that premolar sequences reflect dietary preferences. The functional argument is fraught with problems, however. One has already been noted; in L catta, the posterior permanent premolar does not erupt during the dry season but a t its end. A second problem is that L. fuluus, which eats more leaves than L. catta, does not erupt the posterior premolar first. Finally, even if the correlation holds for most Madagascar lemurs, it does not work for other primate taxa. Among cebids, the probably folivorous Brachyteles arachnoides erupts the permanent premolars in a posteroanterior sequence (della Serra, 19521, like L. catta and Madagascar folivores. In Alouatta, which is also folivorous, the posterior premolar is the last to erupt (della Serra, 1952). The strongly frugivorous Cebus albifions erupts the permanent premolars in a 4-3-2 sequence, like B. arachnoides (Fleagle and Schaffler, 1982). Thus, in New World primates there does not appear to be any correlation between premolar eruption sequences and dietary preference. In summary, the timing of tooth eruption among Madagascar lemurs shows some correlations with behavioral events and changing ecological conditions which arise during the first year and a half of life. The deciduous toothcomb erupts at or shortly after birth but is probably not related to any specific behavioral event. The deciduous chewing teeth erupt at the time when young lemurs are making the transition from a diet of maternal milk to one of solid foods. Growth is rapid and continuous during this period and extends to approximately 6 months of age among the smaller species of the genus Lemur. In L. catta and L. fuluus, permanent tooth eruption begins and the growth rate slows down slightly in advance of the dry season, when leaves gain a n increasing prominence over fruit in the diets of these species. By the TOOTH ERUPTION IN LEMURS 315 middle of the dry season the two anterior tellectual stimulus for undertaking the projpremolars and the permanent anterior den- ect in the first place, and special thanks are tition have erupted; no further eruption oc- warranted for his support. curs until the onset of the following rainy LITERATURE CITED season. The beginning of the new rainy season is Albignac, R (1969) EMvage d'un jeune propitheque, 16murien folivore de Madagascar. Mammalia 33~341accompanied by a n increase in the growth 343. rate of juvenile L catta and L. fulvus, and Chase, JE, and Cooper, RW (1969) Physical growth and coincides with the second wave of permanent dental eruption in a small population of captive born individuals. Am. J. Phys. Anthropol. 30:111-116. tooth eruption, in which the permanent premolars, posterior molars, and upper canine della Serra, 0 (1952) A seqiiencia eruptiva dos dentes definitivos nos simios Platyrrhina e sua interpretaqso appear. The advent of the rainy season aufilogenetica. Anais de Facultade de Farmacia e Odougurs a dietary shift toward increasing contologia de Universidade de Sso Paulo I0:215-296. sumption of fruit and reduction in leaf intake. Eaglen, RH, and Boskoff, K J (1978)The birth and early development of a captive sifaka, Propithecus uerreulwci The data discussed here suggest that the coguereli. Folia Primatol. (Basel) 30t206-219. timing of tooth eruption can be related to Fleagle, JG, and Schaffler, MB (1982) Development and changes in ecology and behavior, a t least for eruption of the mandibular cheek teeth in Cebus ulbithose lemurs whose behavior is reasonably frons. Folia Primatol. masel) 38~158-169. well documented in the wild. At this stage Glassman, DM (1983) Growth and development in the Saddle-Back Tamarin: The sequence and timing of such hypotheses must remain tentative; they dental eruption and epiphyseal union. Am. J. Primaare based on admittedly small samples and tol. 5.51-59. require the juxtaposition of data from captive Kay, RF, Sussman, RW, and Tattersall, I(1978) Dietary animals with events which occur in wild leand dental variations in the genus Lemur, with comments concerning dietary-dental correlations among mur populations. Corroboration of the hyMalagasy primates. Am. J. Phys. Anthropol. 49:119potheses and their further elaboration will 127. require broader sampling of tooth eruption Klopfer, PH, and Dugard, J (1976) Patterns of maternal and growth data, preferably from wild specicare in lemurs. 111. Lemur uuriegutus. Z. Tierpsychol. 40:210-220. mens, of both primarily frugivorous and priKlopfer, PH, and Klopfer, MS (1970) Patterns of matermarily folivorous Madagascar lemurs. nal care in three species of Lemur. I. Normative deDietary hypotheses can also be advanced scription. 2. Tierpsychol. 27t984-996. to account for the sequence of permanent Martin, RD (1972) Adaptive radiation and behavior of premolar eruption in lemurs as well as the the Malagasy lemurs. Philos. Trans. R. Soc. Lond. [Biol] 264B3295-352. timing of eruption. In this case, however, there are several lines of counterevidence Petter-Rousseaux, A (1962) Recherches sur la biologie des Primates inferieurs. Mammalia (Suppl.) 26t1-88. presently available which render such a n ac- Relethford, JH,Coelho, AM, and Lawrence, WA (1982) count tenuous a t best. Still, if the hypothesis Brief report: Age estimation from dental eruption in holds, it can be invoked to account for otherinfant and juvenile baboons (Pupiosp.). Am. J. Primatol. 2~205-209. wise inexplicable parallel sequences of preA (1976) Preliminary observations on the birth molar eruption exhibited by seemingly Richard, and development of Propithecus uerreuuri to the age of remotely related prosimians such as adapids six months. Primates 17:357-366. and ring-tailed lemurs. Schwartz, JH (1974) Dental Development and Eruption ACKNOWLEDGMENTS The research reported here was made possible through the cooperation of the management and staff of the Duke University Center for the Study of Primate Biology and History; among that group, particular thanks are due to David E. Anderson and Katy Ahmann. W.P. Luckett provided helpful suggestions for the preliminary version of this manuscript. R.W. Sussman suggested the possible relationship between eruption patterns and ecological conditions, for which I a m grateful. Matt Cartmill provided the in- in the Prosimians and its Bearing on their Evolution. Ph.D. thesis, Columbia University. Schwartz, JH (1975) Development and eruption of the premolar region of prosimians and its bearing on their evolution. In I Tattersall and RW Sussman (eds): Lemur Biology. New York Plenum Press, pp. 41-63. Sussman, RW (1974)Ecological distinctions in sympatric species of lemur. In RD Martin, GA Doyle, and AC Walker (eds): Prosimian Biology. London: Duckworth, pp. 75-108. Sussman, RW (1977) Socialization, social structure, and ecology of two sympatric species of Lemur. In S. Chevalier-Skolnikoff and F Poirier (eds): Primate BioSocial Development. New York: Garland, pp. 515-528. Tappen, NC, and Severson, A (1971) Sequence of eruption of permanent teeth and epiphyseal union in New World monkeys. Folia Primatol. (Basel)15~293-312.