Dental Eruption Sequence Among Colobine Primates

Dental Eruption Sequence Among Colobine PrimatesKATERINA HARVATI*Ph.D. Program in Anthropology, Graduate School, City University of NewYork; NYCEP; and Department of Vertebrate Paleontology, AmericanMuseum of Natural History, New York, New York 10024-5192

KEY WORDS dental development; folivory; life history

ABSTRACT Dental development is one aspect of growth that is linked todiet and to life history but has not been investigated among colobines since thework of Schultz [1935]. This study establishes the dental eruption sequence forseveral colobine species and compares it to that of other catarrhines. The man-dibles and maxillae of two hundred and four juvenile colobine specimens werescored for presence or absence of permanent teeth and for stages of partialeruption. Eruption was defined as ranging between tooth emergence (any part ofa tooth crown above the alveolar margin) and full occlusion, with three interme-diate levels manifest between these boundaries. In African colobines, repre-sented by C. guereza, C. angolensis and P. badius, M2 erupts before I2, and in C.angolensis it also erupts before I1. The canine is delayed, erupting after thepremolars in females and after M3 in males. Asian colobines show greaterdiversity in eruption sequences. Nasalis shows no early eruption of the molarsand is very similar to Macaca. In Trachypithecus and Pygathrix M2 erupts beforeI2. The canine in Trachypithecus is delayed, erupting after the premolars and, insome males, after M3. In Presbytis M2 erupts before both incisors; M3 eruptsbefore C in both sexes, and often before both premolars. Although the actualtiming of eruption is unknown, all colobine species examined except N. larvatusshowed some degree of relatively early eruption of M2 and M3. The lack of thistendency in Nasalis sets this genus apart from all other colobines represented inthis study. Dental eruption sequence is thought to reflect life history patterns.Early molar eruption in colobines was thought by Schultz (1935) to be a primi-tive character reflecting shorter life history. Faster growth rates found in folivo-rous primates have been interpreted as being related to an adaptation to folivory(Leigh 1994), and early eruption of molars may be part of this dietary special-ization. The relationships between dental development and both diet and lifehistory are investigated. Am J Phys Anthropol 112:69–85, 2000.© 2000 Wiley-Liss, Inc.

The dental development of colobine pri-mates has not been investigated since thework of Schultz (1935) and is largely un-known, as are many other aspects of theirgrowth and life history. Dental developmentand eruption sequences are considered im-portant indicators of life history patterns,and their study can shed light on the evolu-tion of life history in humans and other pri-mates (Smith 1994). This paper aims to es-tablish the dental eruption sequences in

several colobine genera and to comparethem with that of other catarrhines.

Recipient of the 1998 Earnest A. Hooton award.Grant sponsor: Alexander S. Onassis Public Benefit Founda-

tion.*Correspondence to: Katerina Harvati, Department of Verte-

brate Paleontology, American Museum of Natural History, NewYork, NY 10024-5192.E-mail: [email protected] or [email protected]

Received 11 January 1999; accepted 11 December 1999.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 112:69–85 (2000)

© 2000 WILEY-LISS, INC.

In his seminal study, Schultz (1935) ex-amined material of Colobus, Nasalis, andPygathrix following the taxonomy of Elliot(1913). Since he did not specify which spe-cies he studied, it is not clear to which of thetaxa he examined the results of this studycorrespond. Thus the “Colobus” of Schultz(1935) could have included specimens ofboth Colobus and Procolobus as used here,while his “Pygathrix” might have includedTrachypithecus, Presbytis, and Semnopithe-cus as used here. Schultz (1935) concludedthat all three of his colobine genera exhib-ited a common tendency for early eruptionof the second molar. This tendency was lesspronounced in Nasalis and more pro-nounced in Pygathrix, which also showedvery early eruption of the third molar.Schultz (1935) believed that dental eruptionsequences reflect overall growth rates andconsidered that the colobine tendency forrelatively early molar eruption indicated amore primitive dental eruption schedule,and hence a shorter growth period andfaster growth rates, compared to other ca-tarrhines.

More recently, it has been suggested thatdental eruption sequences are indeed verytightly correlated with growth and life his-tory among mammals, but that they do notnecessarily indicate phylogenetic relation-ships (Smith, 1994). Furthermore, the di-etary specializations of colobines and otherfolivorous primates have been implicated infaster growth rates (since folivorous specieswere found to grow faster in body weightthan frugivorous primates of similar bodysize; Leigh, 1994). Such dietary specializa-tions have also been associated with smallerrelative brain sizes in colobines (Clutton-Brock and Harvey, 1980). These findingsseem to indicate that colobines have ashorter life history than other catarrhines.However, very little is known about life his-tory variables such as age at menarche andlifespan in colobines, and virtually no agesof dental eruption are known. It is also notclear whether an accelerated life history isconservative for catarrhines or whether it ispart of an adaptation to folivory.

By increasing the number of taxa exam-ined and by following a more up-to-dateclassification, the present study has been

able to expand on the work of Schultz (1935)and to confirm most of his conclusions. Fur-thermore, it has clarified the patterns oferuption shown by the different colobinetaxa examined and emphasized the vari-ability in dental eruption sequences bothwithin and among species and genera.These eruption sequences are considered inthe context of growth patterns, life historyvariables, and dietary adaptations amongcolobine primates. The results are comparedto those obtained by Schultz (1935).

MATERIALS AND METHODS

The jaws of 204 juvenile colobine primatespecimens from the mammalogy collectionsof the American Museum of Natural History(AMNH) and the National Museum of Nat-ural History (NMNH) were examined, rep-resenting the following genera: Colobus,Procolobus, Nasalis, Simias, Pygathrix,Presbytis, Trachypithecus, and Semnopithe-cus. Species were identified by locality ofcapture following the taxonomy given inNapier (1985) and modified according to theclassification of Oates et al. (1994) (althoughDelson in Oates et al. (1994) recognizesSimias as a subgenus of Nasalis and Tra-chypithecus as a subgenus of Semnopithe-cus). The stage of dental eruption of eachspecimen was described, and a system ofscoring eruption was developed. Zoo speci-mens and specimens of uncertain specificassignment were excluded from the analy-sis. The number of specimens, by sex, foreach taxon is shown in Table 1.

Dental eruption: definition andscoring methods

Past studies of dental development in pri-mates have often relied on longitudinal ob-servations from live animals, either throughdirect observations (Chase and Cooper,1969; Long and Cooper, 1968; Phillips-Con-roy and Jolly, 1988; Reed, 1967; Smith,1994) or from radiographs (Anemone et al.,1996; Kuykendall, 1996). Among studies ofdental eruption sequences that rely on di-rect observations of museum specimensthere is no consensus as to the method ofscoring eruption. In living animals a tooth isconsidered to have erupted if any part of itscrown has pierced the gingiva (Smith,

70 K. HARVATI

1994). This event is the emergence of thetooth. In skeletal material some workersscore a tooth as erupted when its crown hasrisen above the level of the alveolar margin(Schultz, 1935; Thorington and Vorek,1976), while others prefer to restrict thisterm to the stage of full occlusion (Chev-erud, 1981). Here a tooth was scored as“emerging” when any part of the crown hadrisen above the alveolar margin.

It is in many cases unclear whether pre-vious studies of dental eruption sequencehave used intermediate stages of eruption.Thorington and Vorek (1976) did not discussthis point; Cheverud (1981), Glassman(1983), and Smith (1994) only scored teethas unerupted or erupted (present/absent).As is evident from his tables and his com-ments (Schultz, 1935, pp. 520–522; see alsoSchultz, 1942, p. 297), Schultz appears tohave considered the degrees of eruption ofeach tooth in determining the eruption se-quence. In the present study, teeth showingan intermediate level of eruption (between“emerging” and “full occlusion”) were fur-ther scored to 1/3, 1/2, and 2/3 of the way tofull occlusion. When the two sides showeddifferent stages of eruption, the most ad-vanced condition for each tooth was scored,

following Schultz (1935). These intermedi-ate stages of eruption were used in estab-lishing the eruption sequences.

Precedence in the sequence was deter-mined as follows. One tooth was consideredto precede another in the sequence if either:a) one was present and the other absent, orb) both teeth had emerged but there was adifference of at least a half step to full oc-clusion between the two. A strict criterion ofpresence or absence for the establishment ofan eruption sequence is perhaps preferable,particularly when longitudinal data areavailable or when the samples for the spe-cies studied are large, but in the presentstudy two factors made the use of interme-diate stages of eruption necessary: a) thesample of specimens for each genus wassmall, and b) many of the specimens exam-ined showed several teeth in stages of de-velopment intermediate between emer-gence and occlusion, making it difficult toestablish the sequence of eruption by simplyassessing presence or absence. Furtherstudy of wear facets and food staining, aswell as work on live animals or radiographs,will be useful in confirming the results ob-tained in the present study.

The species were combined to representgenera; different species were consideredseparately when the sample size allowed.Specimens of both sexes, as well as speci-mens of unknown sex, were first consideredtogether, and a sequence of eruption wasestablished. Specimens of known sex werethen separated, and any differences in theeruption sequence of the two sexes werenoted. The eruption sequences are pre-sented as “augmented sequences” (Smith,1994), indicating variability among speci-mens of the same taxon. The following con-ventions were used: The order in which asequence is presented was the most com-mon. Although Smith (1994) used bracketsto indicate sequence polymorphisms that oc-cur at high frequencies, in the present studythey indicate any sequence polymorphism.The equal sign (5) between two teeth indi-cates that the two alternative sequences fora particular position occur an equal numberof times. Question marks in the eruptionsequences indicate that no data were avail-able for that position. In the discussion of

TABLE 1. Numbers of specimens for eachtaxon studied

Females MalesUnknown

sex Total

Colobus 20 20 5 45C. guereza 14 13 3 30C. angolensis 6 7 2 15

Procolobus 17 8 4 29P. badius 15 8 4 27P. verus 2 2

Nasalis (larvatus) 4 9 13Simias (concolor) 3 3 6Presbytis 28 28 4 60

P. hosei 12 3 15P. melalophos 7 11 2 20P. rubicundus 3 4 7P. potenziani 1 3 2 6P. frontata 3 4 7P. comata 2 1 3

Pygathrix 6 3 9P. nemaeus 4 1 5P. roxellana 2 2 4

Trachypithecus 16 21 1 38T. cristatus 6 11 17T. phayrei 5 5 10T. pileatus 4 3 1 8T. johnii 1 2 3

Semnopithecus(entellus)

2 2 4

COLOBINE DENTAL ERUPTION SEQUENCES 71

the results, n represents the number of in-formative specimens for the particular posi-tion in the taxon under consideration. Datamatrices for these taxa are presented in theAppendix.

RESULTS

The eruption sequences of the colobinetaxa examined are presented in Table 2.

African colobines (Subtribe Colobina)Colobus. Two species were represented inthis genus, C. guereza and C. angolensis.The sample size was large enough for thetwo species to be considered separately. Thesequences of the two species were slightlydifferent (Table 2). In C. guereza, M2 eruptsbefore I2 in the only specimen availablefor this position (Fig. 1B). In the mandible,the I2 M2 sequence is the only one present(n 5 2).

No specimens show M2 before I1 (n 5 4) orM2 before I1 (n 5 3). The sequence of the

premolars is variable in the maxilla, the twoinformative specimens showing oppositeconditions. In the mandibles in all four spec-imens, P4 erupts before P3. Finally, the po-sition of the third molar is variable both inthe upper and lower dentition. In 6 of 9individuals (67%), M3 erupts before C/,while M3 erupts before /C in 4 of 6 individ-uals (67%). Two specimens (one male andone of unknown sex) out of five show M3erupting even before P3. When the sexes areseparated, it is found that the position of thecanine relative to the third molar is stillpolymorphic for both sexes. However, in fe-males, M3 tends to erupt last in both lowerand upper jaws, after the canine (2 of 3specimens for both jaws). In most males (4of 5), C/ erupts last, after M3, and in allmales (n 5 2), /C erupts after M3 (Figs. 2B,3A).

This pattern could be attributed to sexu-ally dimorphic growth of the canine, eventhough C. guereza is noted for the smalldegree of sexual dimorphism in canine sizeand for the large size of the female canines(Delson, 1973; Lucas and Teaford, 1994).

C. angolensis exhibits a different pattern.The tendency of M2 to erupt early is morepronounced, and this tooth erupts before I1in 3 of 4 individuals in the upper jaw, and inboth lower jaws informative for this se-quence position. Unlike C. guereza, M2erupts before I2 in all specimens in bothjaws (n 5 6 for the maxilla and n 5 4 for themandible). The position of I2 relative to thepremolars is judged polymorphic because inone male specimen, AMNH 52148, both up-per premolars erupted before I2. This spec-imen is the only one in this study to showthis unusual sequence, which occurs at lowfrequencies in chimpanzees, and even lessfrequently in macaques (Smith, 1994). Thesequence between the two premolars is sim-ilar to that of C. guereza: the two informa-tive specimens show opposite conditions inthe maxilla, while in the mandible in allfour specimens, P4s erupt before P3s. Theposition of the canine relative to the thirdmolar seems to vary by sex, as in C. guereza.The only female specimen showing this se-quence position, AMNH 52157, shows M3erupting last in both jaws. No males showedthis position in the maxilla; in the mandible,

TABLE 2. A: Eruption sequences established bySchultz for three colobine genera

(following the taxonomy of Elliot, 1913)

Colobus M1 I1 M2 I2 P3 P4 C M3M1 I1 [M2 I2] P3 P4 [C M3]

Nasalis M1 I1 [I2 M2] [P3 P4] C M3M1 I1 [I2 M2] C? [P3 P4] M3

Pygathrix M1 M2 I1 I2 M3 [P4 P3] CM1 M2 I1 I2 M3 [P4 P3]

B: Eruption sequences for seven colobine taxa(following Oates et al., 1994) as established here

C. guereza M1 I1 M2 I2 [P3 5 P4] [M3 C]M1 I1 I2 M2 P4 [P3 M3 C]

C. angolensis M1 [M2 I1] [I2 P3 5 P4] C M3M1 M2 I1 I2 P4 [P3 M3 C]

Procolobus M1 [I1 M2] I2 [P3 P4] [C M3]M1 [I1 I2 M2] P4 [P3 C M3]

Nasalis M1? I1? I2 M2 P3? P4 C M3M1? I1? I2 M2 [P3? P4 C] M3

Trachypi-thecus

M1 I1 M2 I2 [P3? P4 C] M3M1 I1 [I2 M2] P4 P3 [C M3]

Presbytis M1 M2 I1 I2 [M3 P4 P3 C]M1 M2 I1 I2 [M3 P4 P3] C

Pygathrix M1 [I1 M2] I2 P3? P4 C M3M1 I1 M2 I2 C P3? P4 M3

72 K. HARVATI

both male specimens show M3 erupting be-fore /C. This evidence suggests sexually di-morphic growth of the canine. In one malespecimen, M3 erupted before P3.

In general, the sequences of the two Colo-bus species are similar, and only seem todiffer in the position of M2, which appearsearlier in C. angolensis. It may be, however,that the differences detected between thetwo species are caused by the relativelysmall sample sizes available. The sequenceestablished for C. guereza is similar to thatreported by Schultz (1935) for the genusColobus, but it is not clear which specieswere represented by the specimens that heexamined.

Procolobus. This study included the spe-cies Procolobus (Piliocolobus) badius andProcolobus (Procolobus) verus. P. verus wasrepresented only by two specimens. Eventhough these taxa are distinguished at thesubgeneric level, they were considered to-gether. The combined sequence for Procolo-bus is highly variable, and remains so evenwhen the P. verus specimens are removed.The variability in the sequence thereforedoes not seem to be due to differences be-tween the two taxa. The following discus-sion pertains to the combined sample of Pro-colobus (Table 2). As in C. guereza, the mostcommon sequence in the mandibular denti-tion is I2 M2 (4 of 6 specimens), but theconverse sequence, M2 I2, is the only onepresent in the maxilla (n 5 3). Both jawsshow a slight tendency for M2 to erupt be-fore I1 (1 of 5 specimens in both jaws), asequence that also occurs in C. angolensis ata much higher frequency. The sequence atthe P3/P4 position is variable: P3 erupts be-fore P4 in 2 of 3 specimens, while P4 eruptsbefore P3 in 3 of 5 specimens. Among males,

Fig. 1. Stage of eruption of the maxillary permanentincisors relative to the second molar in three colobinespecies. A: Nasalis larvatus (AMNH 103463, male),showing both central and lateral permanent incisors infull occlusion and emerging second molar. B: Colobusguereza (AMNH 81073, female), showing permanentcentral incisors and deciduous lateral incisors in placeand emerging second molar. C: Presbytis frontata(AMNH 103404, male), showing both central and lat-eral deciduous incisors in place and emerging secondmolar.


M3 erupts before C/ in two specimens eachin the maxilla (n 5 3) and in the mandible(n 5 4). Females tend to erupt M3 last, withM3 erupting before C in only one specimenboth in the maxilla (n 5 7) and in the man-dible (n 5 4). In two additional specimens ofunknown sex, M3 erupts after C/. In 2 spec-imens (one male and one female) out of 7,M3 erupts before P3. /C erupts before both

premolars in one female (AMNH 52317), asequence also observed in female macaquesby Smith (1994). In one male (AMNH52272) /C, as well as both premolars,erupted before M2. This is an unusual se-quence that does not appear in chimpanzeesor pigtail macaques (Smith, 1994).

The remarkable variability observed inthis sequence is not due to differences be-tween the two subgenera included, since thesequence is equally variable when P. badiusis considered alone. However, this high levelof sequence polymorphism might possiblybe due to differences among the P. badiussubspecies included (P. b. temmincki, P. b.tephrosceles, P. b. oustaletti, P. b. tholloni,P. b. badius).

Asian colobines(Subtribe Semnopithecina)

Nasalis. Thirteen Nasalis juveniles wereavailable for study. Based on this smallsample size, a tentative sequence was estab-lished, which is very similar to that of Ma-caca nemestrina established by Smith(1994) in the positions that could be exam-ined (Table 2). No tendency was observedfor M2 to erupt before I2 (Fig. 1A). The twoinformative specimens for this conditionshowed fully occluding I2 combined withemerging M2 in both jaws. The only poly-morphism found in the Nasalis sequenceconcerns the position of /C relative to thetwo premolars, and seems to be related tosexual dimorphism. Both males erupted /Cafter both premolars, while in both femalesthis tooth erupted before both premolars.This polymorphism was also observed in M.nemestrina, where in males the canineerupts either between the two premolars, orbetween P3 and M3, while in females thistooth tends to erupt before the premolars(Smith, 1994). The later eruption of the ca-nine in males suggests a longer growth pe-riod for this tooth, which is probably relatedto the larger size of male canines. M3 wasalways found to erupt last in both males andfemales, and in both jaws. In this respect,Nasalis again resembles Macaca and is un-like several other colobine genera (Fig. 2A).The sequence was not determinable at theM1/I1 and the P3/P4 positions in both jaws.

Fig. 2. Stage of eruption of the maxillary permanentcanine relative to the third molar in a macaque and intwo colobine species. A: Macaca fascicularis (AMNH107566, male), showing the permanent canine (C) al-most fully occluding and emerging third molar. B: Colo-bus guereza (AMNH 52236, female), showing the decid-uous canine (dc) in place and the third molar almosthalfway to full occlusion. C: Presbytis frontata (AMNH103405, female), showing the deciduous canine (dc), aswell as the deciduous premolars, in place and emergingthird molar.

74 K. HARVATI

Schultz (1935) found the eruption se-quence of Nasalis to be similar to that ofother catarrhines, based on a sample ofseven crania. However, he noted a tendencyfor early eruption of the second molar,which he considered a common characteris-

tic of the three colobine genera that he stud-ied. Such a tendency was not observed inthe present study.

Simias. Six specimens of Simias concolorwere examined. It was not possible to estab-

Fig. 3. Stage of eruption of the mandibular permanent canine relative to the third molar in twocolobine species. A: Colobus guereza (AMNH 52236, female), showing the deciduous canine (dc) in placeand the third molar almost in full occlusion. B: Presbytis frontata (AMNH 103405, female), showing thedeciduous canine (dc), the deciduous third premolar in place, emerging fourth premolar, and third molarin full occlusion.


lish the sequence of eruption, since theseindividuals did not show most positions ofinterest. One maxillary and one mandibularspecimen showed I1 erupting before M2. Inthis respect, Simias seems different fromPresbytis or Colobus angolensis, but similarto the other taxa examined here. No infor-mative specimens were available for theI2/M2 position or the P3/P4 position. M3

erupted last in two individuals (one maleand one female), as did M3 in one specimen,a male.

Trachypithecus. This genus was repre-sented in this study by the species T. cris-tatus, T. pileatus, T. phayrei, and T. johnii.Among them only T. pileatus and T. crista-tus were represented by large enough sam-ples to be considered separately. No differ-ences were detected between these species;therefore, all Trachypithecus specimenswere combined. The Trachypithecus se-quence shows a tendency for early eruptionof the second molar, which is more pro-nounced in the maxilla (Table 2). M2 alwayserupts before I2 (n 5 2), while M2 eruptsbefore I2 in 1 of 3 specimens. M2 was neverobserved to erupt before I1 in either jaw.Only one specimen showed the P3/P4 posi-tion. In this individual, P4 erupted first. M3erupted last in both males and females andin both jaws, with the exception of one male(n 5 5), in whom M3 erupted before /C. Intwo male maxillae and one mandible, M3erupted at the same time as C. Finally, inone male specimen (AMNH 113499, n 5 6),C/ erupted before both premolars. This se-quence polymorphism is common in M. nem-estrina females, and its presence in a maleis unusual. The variability indicated aboveinvolving the position of the canine relativeto the premolars is due to this specimen.

Trachypithecus shares with C. guereza amoderate tendency, stronger in the maxilla,for M2 to erupt early, before I2. A weaktendency for early eruption of M3 was alsodetected. This trend is shared with most ofthe other taxa examined in this study.

Presbytis. This genus was represented bythe following species: P. rubicundus, P.melalophos, P. potenziani, P. frontata, P.thomasi, P. hosei, and P. comata. Three spe-

cies, P. melalophos, P. hosei, and P. fron-tata, were represented by large enoughsamples to be considered separately. Allthree showed very similar sequences. Allspecimens were combined and a sequencefor the genus was established (Table 2). TheM2 I1 sequence, which also appears veryfrequently in C. angolensis and rarely inProcolobus, is found in all specimens ofPresbytis (n 5 6 for both jaws). M2 alwaysappears before I2 in both jaws (n 5 17 forthe maxilla, n 5 12 for the mandible) (Fig.1C). P4 always erupts before P3 (n 5 4 inthe maxilla, n 5 5 in the mandible). M3emerges extraordinarily early (Figs. 2C,3B). M3 appears before C in the vast major-ity of specimens (18 of 19, or 95% in themaxilla, and 13 of 15, or 87%, in the man-dible). M3 was found to erupt before C fre-quently also in C. guereza, and less fre-quently in C. angolensis and Procolobus. InPresbytis, M3 also tends to erupt before oneor both premolars in both jaws, but morefrequently in the mandible: M3 appears be-fore P3 in 10 of 17 specimens (59%) in themaxilla and in 10 of 13 specimens (77%) inthe mandible. M3 erupts before P4 in 9 of 17specimens (53%) in the maxilla and in 8 of12 specimens (67%) in the mandible. A ten-dency for eruption of M3 before P3 ispresent in the lower jaws of C. guereza, C.angolensis, and Procolobus, where the M3 P3sequence occurs at much lower frequencies(never exceeding 30%) than those presentedby Presbytis. None of these taxa show thistendency in the upper jaw, nor do they evershow M3 erupting before P4. In this respect,Presbytis is unique among the colobine gen-era studied. The extremely early eruption ofM3 could be due to the small size of thistooth, which is reduced in Presbytis (Oateset al. 1994).

When the sexes are separated, a dimor-phic pattern emerges. In females, M3 tendsto erupt before both premolars and the ca-nine, while in males, M3 tends to erupt afterthe premolars and before the canine. Amongfemales, 8 of 10 specimens show M3 beforeP3; in 7 of 9 (78%), M3 erupts even earlier,before P4; and 9 of 10 show M3 eruptingbefore C/. In the mandible, 8 of 9 females(89%) show M3 before P3; 7 of 9 (78%) showM3 before P4; and 9 of 10 show M3 before /C.

76 K. HARVATI

While in most male specimens M3 erupts be-fore the canine (all 9 specimens in the max-illa, and 3 out of 4 in the mandible), M3 eruptsbefore one or both premolars much less fre-quently than in females: 2 of 7 (29%) show M3

before P3 and M3 before P4; only 1 of 3 showM3 before P3, and none (n 5 2) show M3 beforeP4. Here it is not the position of the caninewhich is sexually dimorphic, since it eruptslast in both sexes. It is rather the position ofM3 which differs between the sexes, erupt-ing earlier in females. This pattern cannotbe explained by longer growth for the malecanines, since there is no difference in therelative position of this tooth, unless thereare marked differences in the timing of itseruption. However, it must be noted thatthis pattern may also be due to species-leveldifferences. Most females in whom the thirdmolar erupts before the premolars belongedto P. hosei, for which a large number offemales was available. There were onlythree male P. hosei, none among them show-ing this sequence position.

This sequence is very similar to that pro-posed by Schultz (1935) for his genus Pyg-athrix (sensu Elliot). It is likely that at leastsome individuals examined in his study ac-tually belonged to Presbytis as used here.

Pygathrix. The species Pygathrix (Pyg-athrix) nemaeus and Pygathrix (Rhinopithe-cus) roxellana were examined. These taxaare distinguished at the subgeneric level,but were pooled here due to the small num-ber of individuals available. The sequenceestablished for this genus (Table 2) showsthat M2 erupts before I2 in both the maxilla(n 5 3) and the mandible (n 5 1). One of 3individuals also shows M2 erupting beforeI1, but the one informative specimen for themandible shows the I1 M2 sequence. Thesequence was not determinable at the P3/P4position. M3 erupts last in both the upper(n 5 1) and the lower (n 5 2) dentition. /Cerupts before both premolars (n 5 1, NMNH258986, a male). This sequence is present inM. nemestrina (Smith, 1994) and in Nasalis,where it usually appears in females. It isalso shown by a single Trachypithecus male,AMNH 113499. The only specimen showingthe eruption sequence in the maxilla (AMNH110456) was a female: both premolars

erupted before the canine. It must be notedthat the sample size for this genus was verysmall. The sequence presented here istherefore only tentative.

Semnopithecus. Four Semnopithecus en-tellus specimens were examined. They pre-sented no information on the sequence oferuption of the incisors and the second mo-lar, or of the two premolars. In 3 of 4 spec-imens (2 females and 1 male), M3 eruptedlast, while in one male M3 erupted before C/.In this specimen M3 also erupted before /C,while in two other individuals (one femaleand one male), M3 erupted last.

DISCUSSION

This study has confirmed the finding ofSchultz (1935) that colobines differ fromother catarrhines in their dental eruptionsequences in that their second and thirdmolars tend to erupt early relative to theother permanent teeth. Most colobine gen-era studied except Nasalis show various de-grees of advancement in the relative erup-tion of the molars: Although Schultz (1935)found that in Nasalis the second molarserupted early, no such tendency was ob-served here. Its eruption sequence as far ascan be determined is identical to that ofMacaca nemestrina. Presbytis shows themost extreme expression of the trend forearly molar eruption, with the second molaralways erupting before both incisors, andthe third molar almost always erupting be-fore the canine and very often before one orboth premolars in both jaws. Colobus, Pro-colobus, Trachypithecus, and Pygathrix allshow intermediate degrees of expression ofthese tendencies (Figs. 1–3). C. guereza andTrachypithecus often have the second molarerupting before the second incisor, butnever before the first incisor. All other taxashow the M2 I1 sequence at various fre-quencies, Procolobus and Pygathrix rela-tively rarely and C. angolensis very fre-quently. Trachypithecus shows a weaktendency for eruption of the third molar be-fore the canine, as does Semnopithecus.This tendency is stronger in Colobus andProcolobus, where the mandibular third mo-lar sometimes erupts even before the thirdpremolar.


Sequence polymorphisms involving theposition of the second molar relative to theincisors are rare in macaques and chimpan-zees. Smith (1994) found that in male Ma-caca nemestrina, M2 erupts before I2 at a2% frequency in both maxillary and man-dibular dentition, while in females it occursat a 2% frequency in the mandible andnever in the maxilla. In Pan troglodytes, anM2 I2 sequence appears at frequencies of28% in the maxilla and 13% in the mandi-ble. Smith (1994) reported no occurrence ofthe M2 I1 sequence in macaques, but foundan incidence of 3% frequency in the maxillaand 7% frequency in the mandible of chim-panzees. Polymorphisms involving the posi-tion of the M3 were not observed amongmacaques or chimpanzees, where this toothalways appeared last.

Dental eruption sequence andlife history patterns

The sequence of dental eruption isthought to reflect life history patterns.Schultz (1935, 1960) believed that in “prim-itive” primates (probably meaning tupaids)the molars were the first permanent teeth toerupt. Only after all the molars had ap-peared did the permanent incisors, premo-lars, and canines replace the deciduousdentition. Among “higher” primates, thetendency to prolong the growth periodcaused the appearance of the molars to bedelayed, while replacement of the deciduousteeth occurred earlier in the sequence. Ashumans have the most prolonged growthperiod among primates, they were alsothought by Schultz (1935, 1960) to be themost “advanced” in their dental eruptionsequence, with the second molar eruptingonly after all the deciduous teeth have beenreplaced. This scheme implied that, at leastamong primates, there is a correlation be-tween phylogeny as represented by evolu-tionary grade, growth prolongation, and rel-ative timing of eruption of the molars.Schultz (1935) believed that the colobineeruption sequence, showing a relativelyearly eruption of the molars, was primitivefor catarrhines. Rather than emphasizingthe dichotomy between primitive and ad-vanced, Smith (1994) differentiated be-tween fast-growing and slow-growing mam-

mals and pointed out that eruptionsequences probably do not reflect phyloge-netic relationships. She agreed with Schultz(1935) that in fast-growing mammals themolars erupt first and then the rest of thepermanent dentition appears, while in slow-growing mammals, such as humans, lateeruption of the molars relative to the per-manent incisors and premolars occurs be-cause they tend to replace the deciduousdentition first and then add the distal mo-lars. This fact is explained, in her view, bythe need to maintain functional dentitionover a much longer period of growth. If den-tal eruption sequence reflects life history,the early eruption of the colobine molarsprobably indicates faster growth rates andshorter life history phases compared toother catarrhines, but it is not necessarily aprimitive retention.

It is not clear whether colobines show ageneral acceleration of life history. Data onages of dental eruption and on other lifehistory variables, such as age at menarcheand lifespan, are known for very few colo-bine species. Leigh (1994) found that colo-bines and other folivorous primates tend togrow faster in body weight, and to ceasegrowth relatively earlier, than frugivorousprimates of similar size. In her study of T.cristatus males, Wolf (1984) found thatthese animals completed their dental devel-opment at an average age of 3.75 years. Bycomparison, the male Macaca fascicularis, aslightly smaller animal (Smith and Jungers,1997), completes its dental development af-ter 5.5 years, a much later age (Smith et al.,1994). Menarche is known to occur between25.8 and 29 months of age (Sommer et al.,1992) in free-ranging Semnopithecus entel-lus entellus females, at a body size of about10 kg (Smith and Jungers, 1997). Wild Pa-pio hamadryas cynocephalus females, at aslightly larger body size of about 12 kg(Smith and Jungers, 1997), reach menarchemuch later, between 48 and 66 months (Alt-mann and Altmann, 1981). The smaller Ma-caca mulatta females (5.37–8.8 kg, Smithand Jungers, 1997) reach menarche slightlyearlier, between 24.1 and 27.8 months, incaptivity (Van Wagenen, 1952; Catchpoleand Van Wagenen, 1975). It is difficult todetermine whether the differences in these

78 K. HARVATI

life history variables are as large as wouldbe expected given the differences in bodysize between the taxa involved, but the lim-ited available evidence suggests that atleast some colobines may be characterizedby a relatively accelerated life history. Colo-bines were also found to have a smallerbrain size relative to other anthropoids(Clutton-Brock and Harvey, 1980; Harveyet al., 1987; but note that the body massestimates used by these authors have beenquestioned by Smith and Jungers, 1997). Asbrain size tightly correlates with other lifehistory variables, such as body weight, ageat weaning, and age at first breeding(Smith, 1989a,b), this finding also points toa relatively accelerated life history.

Dental eruption sequence and othervariables

The faster growth rates found in somecolobine species have been thought by Leigh(1994) to be related to their folivorous di-etary adaptation. Folivory has also been im-plicated in the smaller relative brain sizefound in the subfamily (Clutton-Brock andHarvey, 1980; Harvey et al., 1987). Colo-bines are known for their folivorous dietaryspecializations, and perhaps early molareruption is part of this adaptation ratherthan just a side effect of faster growth rates.A folivorous diet may require earlier deploy-ment of molars for processing leaves. Accel-erated molar development was found byDirks (2000) in the folivorous species Sem-nopithecus entellus and Hylobates syndacty-lus, when compared to frugivorous speciesof the same family in her study of histolog-ically determined chronology of dental de-velopment. Folivory was also thought to ex-plain early dental development in leaf-eating lemurs by Godfrey (Seachrist, 1996).However, I have shown that, within colo-bines, the taxa with earliest molar appear-ance are not necessarily the most folivorous.Presbytis, the genus with the relatively ear-liest eruption of the molars, is less folivo-rous than some of the other colobines exam-ined here, such as Trachypithecus andColobus guereza (Lucas and Teaford, 1994;Bennet and Davies, 1994), both of whichshow a much less pronounced tendency forearly molar appearance. On the other hand,

Nasalis, whose diet comprises fruit, seeds,young leaves, and a very small component ofmature leaves (Bennett and Davies, 1994),shows no differences in its dental eruptionsequence from a macaque as far as can bedetermined. Its eruption sequence could berelated to its selective feeding habits, or toits large body size.1

Nasalis is set apart from all the othercolobine taxa examined here, both Asianand African, by the lack of any tendency forearly eruption of the molars. This findingcould also be interpreted as supportingGroves (1989), who suggested that the pro-boscis monkey is the sister group to all othercolobines. In this interpretation the erup-tion sequence of Nasalis and Macaca wouldbe primitive for catarrhines, while those ofthe other colobines would be derived, withPresbytis showing the most derived erup-tion sequence. However, as only a smallnumber of Nasalis specimens were avail-able for this study, further work is needed toconfirm this result, as well as to determinethe usefulness of eruption sequences in phy-logenetic analyses (Smith, 1994).

This study found that colobines tend toerupt the fourth premolar before the third.The P4 P3 sequence was the predominantcondition in Colobus, Trachypithecus, andPresbytis, and also occurred often in Pro-colobus. Schultz (1935) noted the variabilityin the P3/P4 position, but found the P4 P3sequence to be predominant only in Pygath-rix (sensu Elliot, 1913, including Trachyp-ithecus, Presbytis, and Semnopithecus asused here). The P4 P3 sequence polymor-phism was found to occur at high frequen-cies in both macaques and chimpanzees bySmith (1994), who noted that the two pre-molars often erupt very close to each other.Therefore, the P4 P3 sequence is by nomeans unusual in catarrhines. Claims thatsuch a sequence indicates a platyrrhine lifehistory (Simons and Rasmussen, 1996),characterized by short offspring dependency

1However, there does not seem to be a direct relationshipbetween early molar eruption and size. Although the smallestcolobine, Presbytis, shows the earliest placement of the molars,and the largest, Nasalis, does not show this tendency at all,Pygathrix, also a large colobine, shows early eruption of thesecond molar.


periods and early sexual maturation, arenot substantiated.

Sexual dimorphism in the dental eruptionsequence was found in several of the colo-bine genera studied, and it usually involvedthe position of the canine. No sexually di-morphic pattern involving the position ofthe premolars relative to each other wasobserved. The position of the canine wasalso found to be dimorphic in macaques. InM. nemestrina males, the canine tends toerupt after both premolars, while femalesshow canine eruption before the premolars(Smith, 1994). A similar pattern was ob-served here in Nasalis, suggesting a sexu-ally dimorphic growth trajectory of the ca-nine very similar to that observed in M.nemestrina. All other genera studied showeda delay of the canine relative to the premo-lars in both males and females, with Cerupting after P3 and P4. Sexual dimor-phism in the eruption sequence involves theposition of the canine relative to the thirdmolar. In C. guereza males the canine tendsto erupt after the third molar, while in fe-males the third molar tends to erupt last. Asimilar sexually dimorphic pattern is sug-gested, but could not be convincingly dem-onstrated, in C. angolensis, Procolobus, Tra-chypithecus, and Semnopithecus. Within thegenus Presbytis, the third molar tended toerupt in females before one or both of thepremolars, as well as before the canine,while in males the third molar tended toerupt before the canine but after the premo-lars. Here it is the position of the third mo-lar which is sexually dimorphic, eruptingearlier in females. This pattern cannot beexplained by longer growth for the male ca-nine, since this tooth erupts last in bothsexes, but may be related to the reduced sizeof the third molar in this species.

The subtribe Semnopithecina (Asian colo-bines) encompasses much greater diversityin dental eruption sequences than does theAfrican subtribe (Colobina), probably re-flecting the much greater taxonomic andecological diversity of the Asian group (Ben-nett and Davies, 1994; Brandon-Jones,1984; Oates et al., 1994; Oates, 1994). Se-quence variability is also pronounced withinthe individual colobine taxa examined. Inmost cases this does not appear to be due topooling of species into genera for analysis,

but larger samples are needed to resolvethis question.

CONCLUSIONS

This study has shown that at least somecolobine genera exhibit a dental eruptionsequence that differs from that of other ca-tarrhines, including Macaca, Papio, andPan, as was previously reported by Schultz(1935). Furthermore, it has demonstratedthat there is great variability among colo-bine genera in this sequence, with differ-ences sometimes appearing at the specieslevel. All colobine genera examined here,except Nasalis, showed an early eruption ofthe second molar, before the second incisorand sometimes before the first incisor. Fur-thermore, in Presbytis, and often Colobus,Procolobus, and Trachypithecus, the thirdmolar also erupted at a very early position,before the canine and sometimes even be-fore the premolars. The sequence of erup-tion of the two premolars was variable, withthe fourth premolar usually erupting beforethe third. Early molar eruption in colobinesis thought to be related to faster growthrates and an accelerated life history(Schultz, 1935; Smith, 1994). Data on lifehistory variables exist only for very few spe-cies, but they seem to confirm this hypoth-esis. They also indicate that colobine pri-mates grow faster than frugivorousprimates of similar body size (Leigh, 1994).These findings suggest that faster growthrates may be part of their folivorous adap-tation. Folivorous primates are also thoughtto develop their molars faster than frugi-vores (Dirks, 2000). Early molar eruption incolobines might also be related to folivory.However, within the subfamily, variation ineruption sequences among different colo-bine taxa is not consistent with this hypoth-esis.

The relationships between dental erup-tion sequence and diet, and between dentaleruption sequence and life history, cannotbe convincingly demonstrated at present. Itappears likely that dental development re-flects a compromise between constraints ofphylogeny, size, facial architecture, anddiet. As always, more data for actual erup-tion ages, growth, and life history areneeded to resolve these questions.

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ACKNOWLEDGMENTS

I thank Dr. R.D. MacPhee of the Depart-ment of Mammalogy, AMNH, and Dr. R.Thorington and Linda Gordon of the De-partment of Vertebrate Zoology, NMNH, fortheir permission to examine the primateskeletal collections in their care. I alsothank Dr. Sara Stinson, Dr. Eric Delson, Dr.John Oates, Dr. Patrick Gannon, WendyDirks, Lorraine Meeker, and Chester Tarkafor their help during the preparation of thispaper, as well as one anonymous reviewerand Dr. Holly B. Smith for their helpfulcomments and suggestions.

APPENDIX

The data were tabulated into pairwise se-quences for each taxon and presented inmatrices showing the frequency of both al-

ternative sequences for any two teeth (i.e., Abefore B or B before A). Similar matriceswere used by Smith (1994) to illustrateeruption sequence polymorphisms and theirfrequencies in humans, macaques, andchimpanzees. The sequence shown acrossthe top and down the left side of the matri-ces is the eruption sequence of Macaca nem-estrina, as presented in Smith (1994): M1 I1I2 M2 P3 P4 C M3. This sequence is alsopresent in M. mulatta, M. fuscata, Papiohamadryas, and Pan troglodytes (Smith etal., 1994; Smith, 1994), and is thought tocharacterize many anthropoids (Schultz,1935). It was used here as a baseline inorder to show clearly and in summary thedifferences between the macaque sequenceof dental eruption and that of the colobinesexamined.


Appendix

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Appendix (continued)

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Appendix (continued)

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Dental Eruption Sequence Among Colobine Primates

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