American Journal of Primatology 61:29–40 (2003) RESEARCH ARTICLE Effect of Diet on Dental Development in Four Species of Catarrhine Primates WENDY DIRKSn Department of Anthropology, Division of History and Social Science, Oxford College of Emory University, Oxford, Georgia In this study, dental development is described in two pairs of closely related catarrhine primate species that differ in their degree of folivory: 1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental development to determine how dental development is accelerated in the more folivorous species of each pair. Although anterior tooth formation appears to be unrelated to diet, both S. syndactylus and S. entellus initiate the slowest-forming molar earlier than the related less-folivorous species, which supports the hypothesis that dental acceleration is related to food processing. S. syndactylus initiates M2 crown formation at an earlier age than H. lar, and S. entellus initiates and completes M3 at an earlier age than P. h. hamadryas. Similar stages of M3 eruption occur earlier in the more folivorous species; however, the sex of the individual may also play a role in creating such differences. Although the age at M3 emergence is close to that reported for the end of body mass growth in lar gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence may not be coupled to body mass growth in siamangs. Am. J. Primatol. 61:29–40, 2003. r 2003 Wiley-Liss, Inc. Key words: dental development; folivory; Hylobates; Symphalangus; Papio; Semnopithecus Contract grant sponsor: NSF; Contract grant number: SBR-9700822; Contract grant sponsors: James Arthur Dissertation Fellowship; New York University Graduate School of Arts and Science; Elizabeth S. Watts Fellowship in Nonhuman Primate Growth and Development, American Society of Primatologists. n Correspondence to: Wendy Dirks, Oxford College of Emory University, 100 Hamill St., Oxford, GA 30054. E-mail: email@example.com Received 10 January 2003; revision accepted 11 July 2003 DOI 10.1002/ajp.10106 Published online in Wiley InterScience (www.interscience.wiley.com). r 2003 Wiley-Liss, Inc. 30 / Dirks INTRODUCTION Several studies of primate ontogeny and life history have discussed the relationship between diet and growth [Altmann, 1998; Janson & van Schaik, 1993; Leigh, 1994]. Janson and van Schaik  suggested that the slow growth of primates during the long juvenile period from weaning to first reproduction is a result of increased ecological risks during that stage. Leigh  found that folivores grow more rapidly than frugivores, and suggested that this is due to decreased ecological risk in folivores. He proposed that juvenile folivores require acceleration of dental development to process leaves in seasonal environments, and that their rapid growth in body mass allows for this through the correlation of skeletal growth, size increase, and dental maturation. Studies of dental emergence have demonstrated this acceleration of dental development in folivores relative to that of nonfolivores [Eaglen, 1985; Godfrey et al., 2001; Harvati, 2000; Taylor, 1997]. Histological methods can demonstrate a more precise chronology of acceleration during the developmental period, as well as highlight aspects of variation; however, they generally are not applied to large sample sizes and thus preclude broad generalizations. In this study, histological methods were used to reconstruct dental development in four species of catarrhines to examine the effect of diet on dental development. The ages at initiation and completion of the crowns, and the rate of root growth are compared in a small sample comprised of two closely related hominoids: the highly frugivorous Hylobates lar and the more folivorous Symphalangus syndactylus [Chivers, 1972; Curtin & Chivers, 1978; Palombit, 1997]. Dental development is also compared in two cercopithecoids with fairly eclectic diets, which differ in their degrees of folivory: Papio hamadryas hamadryas and Semnopithecus entellus [Bauchop, 1978; Bennett & Davies, 1994; Hladik, 1977; Kar-Gupta & Kumar, 1994; Koenig et al., 1997; Nagel, 1973; Nystrom, 1992; Ripley, 1965, 1970]. METHODS Study Sample The specimens used to reconstruct dental development are listed in Table I. The generic distinction between the hylobatids follows Schultz  and Roos and Geissmann . Additional details of dental development in H. lar NYU008 and P. h. hamadryas 73261 and 73436 that were not considered in this study can be found in Dirks  and Dirks et al. . Only permanent mandibular teeth were used in the analysis. Reconstruction of Dental Development Dental development was reconstructed using the incremental growth markers that are visible in polarized light in the enamel and dentine. These increments include daily cross striations and longer period striae of Retzius in enamel, as well as the corresponding daily von Ebner and longer period Andresen lines in dentine [Dean, 1995, 2000]. The method used for reconstruction of dental development in H. lar NYU008 is given in Dirks  and Dirks et al.  for P.h. hamadryas 73436 and 73261. Dental development in S. syndactylus 1993 was reconstructed using the method described by Reid and coworkers . Dental development in all of the other specimens except H. lar AS1627 was reconstructed in a similar manner using digital images generated with a Leitz Laborluxs 12 Pol S microscope. All measurements and counts of growth increments were made NYU008 NYU011 NYU029 AS1627 1993 1728 73436 73261 845/70 H. lar H. lar H. lar H. larc S. s. syndactylusd S. syndactyluse P. h. hamadryasf P. h. hamadryasg S. e. priam c b Developing mandibular teeth only. Not available. C1, M33 erupting. d rdi2 in occlusion, LI2 erupting. e I1 missing, M3 erupting. f M2 erupting. g M3 erupting. a Specimen Species Unknown Unknown Unknown Male Unknown Female Female Female Female Sex Unknown Unknown Unknown Thailand Sumatra Unknown Ethiopia Ethiopia India Origin Lower dentition I1–2dc1–dp4M1 I1-M3 I1–2dc1-dp4M1 I1-M3 I1–2dc1-dp4M1 I2-M3 I1-M1 I1-M3 I1-M3 Upper dentition I1di2-dp4M1 I1-M3 N/Ab I1–2dc1P3–4M1–3 I1i2dc1-dp4M1 N/Ab I1-M1 I1-M3 I1-M2 C1P3–4 None C1M2–3 None C1-P4M2–3 None M3 None None Tooth germsa I1–2P4M1–2 C1 I1-M3 P4-M3 I1-M3 I2-M3 I1-M3 I1-M3 I1-M3 Teeth used TABLE I. Description of Specimens Used in Reconstructing Dental Development in Hylobates lar, Symphalangus syndactylus, Papio hamadryas hamadryas, and Semnopithcus entellus priam Diet and Dental Development / 31 32 / Dirks using the public domain NIH Image Version 1.61 (developed at the U.S. National Institutes of Health and available on the Internet at http://rsb.info.nih.gov/nihimage). Details are given in Dirks . Dental development in H. lar AS1627 was reconstructed in the same manner using Improvision Openlab 2.0.7 image analysis software with a Zeiss Universal photomicroscope. Four of the specimens (H. lar AS1627, S. syndactylus 1728, P. hamadryas 73261, and S. entellus 845/70) were in the process of M3 eruption at the time of their death. Both hylobatids were at similar stages, with cusp tips just beginning to emerge above alveolus, and both cercopithecids were also at comparable stages, with mesial cusps below the level of the occlusal plane, and the distal cusps just emerging. The male lar gibbon differed from the other three specimens (all female) in that their mandibular canines had fully erupted, while his canine cusp tips were just beginning to emerge. The age at death in these specimens was determined by using the growth increments visible in the roots, and adding the root formation time to the age at which crown formation was complete. To determine the extension rate (the rate at which the root elongated), the length of the root was divided by the total number of days of root formation. This provides a crude estimate of extension rate for comparative purposes only, because root extension does not proceed at a steady pace as the root forms [Beynon et al., 1998; Dean, 1995, 2000; Dean & Scandrett, 1995]. RESULTS The estimated ages at initiation and completion of tooth crowns are given in Table II. The age at initiation for I1 in S. entellus 845/70 is a minimum, based on the assumption that M1 initiates at around birth, as the cusp was too worn to indicate a more exact age. In all the other specimens, I1 precedes initiation of I2, and this is likely to be the case in S. entellus 845/70 as well. The estimated age at initiation of P4 in S. syndactylus 1728 is also a minimum, as cuspal enamel was lost during preparation. The age at initiation and completion of crown formation was similar among individuals of the same species. The greatest disparity for crown initiation within a species was in the age at initiation of M3 in Hylobates lar NYU029 and AS1627. However, H. lar NYU029 is a captive individual of unknown sex, while AS1627 is a wild-caught male. This difference may be related to earlier initiation due to captivity, or H. lar NYU029 may be a female. The sequence of initiation and completion of incisors, canines, and premolars differed among all four species; however, incisor initiation always preceded premolar initiation. The chronology of development of these teeth appears to be unrelated to diet, since there are no obvious similarities between siamangs/ langurs and baboons/lar gibbons in terms of such development. The molar sequence was the same in all four species. Relative to the baboon, however, the langur exhibited accelerated initiation and completion of M3. Relative to the gibbon, the siamang had accelerated initiation, but not completion, of M2. This acceleration of M2 initiation was apparent even when the variation between individuals was considered. Figure 1 illustrates the chronology of molar development in each individual in the study in which the third molar had initiated. Table III summarizes formation times for each completed tooth crown in all of the specimens used in the study. For all teeth, crown formation times were shorter in langurs than in baboons. However, there was no consistent pattern of differences in crown formation times between the two hylobatid species. In S. syndactylus 1728, M2 took longer to form than either M1 or M3, while in H. lar AS1627, M3 took longer to form than either of the other molars. In both folivores, 0.60–3.29 0.62–3.00 0.23–1.50 P. h. hamadryas 73436f 73261f S. e. priam 845/70g 0.17–1.65 0.69–3.33 0.65–3.19 0.36–2.04 0.38–2.08 0.30–2.08 0.38–1.89 – I2 0.42–2.20 0.73–3.90 0.71–3.98 0.19–incg 0.25–3.65 – 0.34–incg – C1 0.35–2.21 1.10–3.21 1.10–3.10 0.56–3.08 0.56–3.29 – 1.35–2.58 – P3 0.68–1.80 1.48–3.29 1.54–3.17 0.99–2.69 1.08–2.46 1.27–2.54 1.30–2.65 1.48–3.05 P4 0.00–0.89 (–0.10)–1.38 (–0.10)–1.35 (–0.13)–1.36 (–0.18)–0.92 (–0.04)–1.12 (–0.10)–1.02 0.00–1.10 M1 1.13–2.45 1.38–3.12 1.35–2.88 0.66–2.49 0.51–2.32 1.01–2.17 0.98–2.57 1.28–2.42 M2 2.21–3.73 3.65–inch 3.75–5.71 2.61–inch 2.36–3.50 – 2.24–inch 2.94–5.00 M3 c b M1 based on hypoconid; M2 based on entoconid [see Dirks, 1998]. M1 based on unidentified mesial cusp (initiation) and entoconid (completion); M2 and M3 based on protoconid. M1 and M2 based on hypoconid, M3 based on entoconid. d M1 based on protoconid (initiation) and hypoconid (completion); M2 and M3 based on protoconid. e M1 based on entoconid (initiation) and metaconid (completion); M2 based on protoconid (initiation) and hypoconid (completion); M3 based on metaconid (initiation) and hypoconid (completion). f All molars based on protoconid [see Dirks et al., 2002]. g M1 based on entoconid; M2 based on protoconid; M3 based on protoconid (initiation) and hypoconid (completion). h Incomplete at death. a 0.32–2.25 – (–0.01)–1.42 0.02–1.54 – H. lar NYU008a NYU029b AS1627c S. syndactylus 1993d 1728e I1 Specimen TABLE II. Estimated Ages at Initiation and Completion of Crowns in Hylobates lar, S. syndactylus, Papio h. hamadryas, and Semnopithecus entellus priam in years Diet and Dental Development / 33 34 / Dirks M1 P. hamadryas 73436 M2 + M3 M1 P. hamadryas 73261 M2 M3 M1 S. entellus 845/70 M2 Tooth Type M3 M1 H. lar NYU029 M2 + M3 M1 H. lar AS1627 M2 M3 M1 M2 S. syndactylus 1993 + M3 M1 S. syndactylus 1728 M2 M3 -1.00 0.00 1.00 2.00 3.00 4.00 5.00 6.00 7.00 Age (Years) Fig. 1. Bar charts illustrating age at initiation and completion of molar crown formation in Papio hamadryas hamadryas, Semnopithecus entellus, Hylobates lar, and Symphalangus syndactylus individuals in which third molar formation had initiated. Bars represent M1–M3 in each individual. Black is cusp formation, light gray is imbricational (lateral and cervical) enamel formation, and dark gray is total crown formation. Plus signs indicate incomplete crown at death. the formation of the slowest-forming molar appeared to be accelerated relative to that in the less folivorous species. For one specimen of each species, Table IV lists the age at which M3 was erupting at the time of death. Table IV also includes the length of the erupting M3 roots as a proportion of the total length of the complete M2 roots, as well as the average daily extension rate of the distal M3 root. The larger, more folivorous female siamang was a year younger than the male lar gibbon at a comparable stage of M3 eruption. The more folivorous female Hanuman langur was 2 yr younger than the female hamadryas baboon at comparable stages of M3 eruption. However, in both pairs the folivore had a slower average root extension rate, which suggests that it is the difference in the chronology of crown formation, rather than root extension, that creates accelerated molar development in folivores. Although the average extension rate in the mesial M3 roots could not be determined in all of the specimens due to the plane of section, an average extension rate of 17.6 mm per day was determined in the mesial M3 root of S. entellus 845/70. Root extension was faster in both cercopithecids than in the hylobatids, which points to phylogenetic effects on root growth rather than dietary effects. Cercopithecids may simply have faster rates of root growth than hominoids, regardless of diet. DISCUSSION Dietary studies indicate that although gibbons can spend 22–25% of their feeding time consuming young leaves, their diets are largely based on ripe fruit, Diet and Dental Development / 35 TABLE III. Estimated Crown Formation Times in Hylobates lar, S. syndactylus, Papio hamadryas hamadryas, and Semnopithecus entellus priam in years Specimen I1 I2 C1 P3 P4 M1 M2 M3 H. lar NYU008a NYU011b NYU029c AS1627d 1.43 – 1.52 – 1.78 – 1.51 – – 3.08 – – – – 1.23 – 1.27 – 1.35 1.57 1.16 – 1.12 1.10 1.16 – 1.59 1.14 – – – 2.06 S. syndactylus 1993e 1728f 1.93 – 1.68 1.70 – 3.40 2.52 2.73 1.70 1.38 1.49 1.10 1.83 1.81 – 1.14 P. h. hamadryas 73436g 73261g 2.69 2.38 2.64 2.54 3.17 3.27 2.11 2.00 1.81 1.63 1.48 1.45 1.74 1.53 – 1.96 S. e. priam 845/70h 1.27 1.48 1.78 1.86 1.12 0.89 1.32 1.52 a M1 based on hypoconid; M2 based on entoconid [see Dirks, 1998]. C1 based on worn specimen; minimum estimate. M1 based on unidentified mesial cusp (initiation) and entoconid (completion); M2 and M3 based on protoconid. d M1 and M2 based on hypoconid, M3 based on entoconid. e M1 based on protoconid (initiation) and hypoconid (completion); M2 and M3 based on protoconid. f M1 based on entoconid (initiation) and metaconid (completion); M2 based on protoconid (initiation) and hypoconid (completion); M3 based on metaconid (initiation) and hypoconid (completion). g all molars based on protoconid [see Dirks et al., 2002]. h M1 based on entoconid; M2 based on protoconid; M3 based on protoconid (initiation) and hypoconid (completion). b c TABLE IV. Root Development and Age at M3 Emergence Based on Age at Death in Specimens of Hylobates lar, S. syndactylus, Papio hamadryas hamadryas, and Semnopithecus entellus priam Specimen H. lar AS1627 S. syndactylus 1728 P. h. hamadryas 73261 S. e. priam 845/70 Mesial root length (mm) Proportion formed Distal root length (mm) Proportion formeda Average extension rate (mm/day)b, c Age at death (yrs) 2.80 5.29 – 6.16 0.45 0.55 – 0.71 2.78 2.57 7.55 3.88 0.44 0.27 0.73d 0.48 6.8 4.3 19.9 11.4 6.1 5.2 6.8 4.7 a Based on total length of M2 root; length M3/length M2. Microns per day, averaged over total period of root formation (see text for details). Based on distal root. d Based on M2 mesial root. b c especially figs [Bartlett, 1999; Ellefson, 1974; Palombit, 1997; Raemakers, 1984; Ungar, 1993]. Siamangs are more folivorous, but their diet also includes a high proportion of figs and other fruits [Chivers, 1972, 1974; Gittins & Raemaekers, 1980; MacKinnon & MacKinnon, 1980; Palombit, 1997]. The amount of fruit in the diet of both lar gibbons and siamangs varies according to its abundance; however, where they are sympatric, the siamang always includes more leaves in 36 / Dirks its diet–ranging from 16% of feeding time in some studies to 44% of the yearly diet in others [MacKinnon & MacKinnon, 1980; Palombit, 1997; Raemakers, 1984]. Even though lar gibbons (mean female body mass=5.34 kg) are approximately half the size of siamangs (mean female body mass=10.7 kg) in the Sumatran subspecies [Smith & Jungers, 1997], it may take as long (or longer) for a crown to form in gibbons than it does in siamangs. In addition, molar emergence appears to be completed a year earlier in female siamangs than in male lar gibbons. The sample in this study was too small to allow the effect of sex on differences in molar emergence to be taken into account. Nevertheless, the results support the hypothesis that dental development is accelerated in the more folivorous siamang. Figure 1 shows intraspecific variation in ages at onset and completion of crown formation. The greatest variation is in the degree of overlap between the end of M2 crown formation and the onset of M3 crown formation. H. lar NYU029 and S. syndactylus 1728 show overlap, while H. lar AS1627 and S. syndactylus 1993 do not. A previous study found no evidence of overlap in H. lar NYU008 [Dirks, 1998]. Some of this variation may reflect the fact that not all cusps were used in determining crown formation (Table II). If all cusps for each tooth were used, there would be less time between the completion of M2 and the initiation of M3, as cusp formation is not simultaneous [Dirks, 2001]. Another possible reason for the observed variation may be differences between the sexes. If this is the case, it is possible that both H. lar NYU029 and S. syndactylus 1728 are female, and H. lar NYU008, H. lar AS1627, and S. syndactylus 1993 are male. The only two specimens of known sex were S. syndactylus 1728 (a female with overlap in M2 and M3 development) and H. lar AS1627 (a male without overlap). It seems less likely that these differences are due to more rapid dental development in captive animals compared to wild animals [Phillips-Conroy & Jolly, 1988], because both NYU029 (with overlap in M2 and M3 development) and NYU008 (without overlap) [Dirks, 1998] were captive individuals. Both S. syndactylus 1728 and H. lar AS1627 were wild-caught individuals. Although both hamadryas baboons and Hanuman langurs have highly eclectic diets, langurs consume a higher proportion of mature leaves. The baboons in this study were from the Awash National Park hybrid zone, an area of contact and gene flow between populations of hamadryas and anubis baboons [Dirks et al., 2002]. Baboon diets in the hybrid zone are heavily based on flowers and beans of the Acacia species, but also include grass shoots, sedge roots, fruits, and some leaves [Nagel, 1973]. These diets are similar to hamadryas diets elsewhere in Ethiopia, where beans and dry leaves of acacia account for 84% of the diet during the dry season, with a shift to acacia flowers and grass seeds during the long rains [Kummer, 1968]. The diet of Semnopithecus entellus priam has not yet been studied; however, the yearly diet of the closely related subspecies S.e. thersites consists of 21% mature leaves, 27% new leaves, 7% flowers, and 45% fleshy fruits (especially figs) [Hladik, 1977]. Hanuman langurs and baboons are similar in body mass, although both species vary considerably in terms of geographic range. The mean female body mass of S.e. priam is 9.9 kg [Napier, 1985; Roonwal, 1981]. The mean female body mass of baboons from the Awash hybrid zone has also been reported to be 9.9 kg [Phillips-Conroy & Jolly, 1981]; however, this was determined during a drought, and it is believed that the mean female body mass is actually slightly heavier (C.J. Jolly, personal communication). Nevertheless, the total period of crown formation, as well as crown formation time for individual teeth, is much shorter in the langur than in the baboon. Diet and Dental Development / 37 Smith and coworkers established a correlation between the timing of the emergence of the first permanent molar and weaning [Smith, 1989a, b, 1992; Smith et al., 1994]. The emergence of the permanent molars is critical to food processing, and the need for folivores to accelerate molar development has been addressed in a number of previous studies. Eaglen  suggested that variation in the timing of tooth emergence in Malagasy lemurs is related to differences in seasonal and interspecific differences in the degree of folivory during ontogeny. Leigh  found that body mass increased more rapidly in folivores during ontogeny than in nonfolivores of similar adult body mass, and that it may be more efficient for relatively larger subadults to obtain nutrients from leaves during weaning and periods of seasonal dependence on foliage. He further suggested that a genetic correlation between dental development and skeletal/body growth, and the need to process leaves at relatively young ages leads to accelerated dental development. He proposed that reduced ecological risk in folivores [Janson & van Schaik, 1993] permits an acceleration in growth relative to that in nonfolivores. The age at emergence of the third molars in the specimens in this study was consistent with data on body mass growth in all species except the siamangs. Captive lar gibbons reach adult size at ~6 yr of age [Kirkwood & Stathatos, 1992; Leigh & Shea, 1995], while siamangs grow until they reach the age of B7.5 yr [Leigh & Shea, 1995]. The earlier emergence of M3 in the siamang is consistent with the hypothesis that folivores experience accelerated dental development, but suggests that dental development and body mass growth are uncoupled in siamangs. This uncoupling of dental development and body mass was recently demonstrated in a histological study of dental development in a subfossil lemur [Schwartz et al., 2002]. Wild hamadryas baboons do not change in appearance after ~5.6 years of age; however, body mass may increase until B7 yr [Sigg et al., 1982]. Female Hanuman langurs appear to reach adult body mass at about 4.5–5 yr in captivity and at Pollanaruwa [Leigh, 1994; Ripley, 1965]. M3 emergence is close to the end of body mass growth in both cercopithecids. The notion of accelerated dental development has also been explored in studies of dental emergence [Godfrey et al., 2001; Harvati, 2000]. Harvati  examined dental emergence sequences in seven colobine taxa, and found that molar emergence occurred earlier in the overall sequence in six of these taxa than it did in macaques. However, the most folivorous taxon did not exhibit the greatest degree of accelerated molar emergence, and it was suggested that life history, body size, phylogeny, and facial morphology may also play a role [Harvati, 2000]. Godfrey and coworkers have conducted a number of studies on accelerated dental development in a wide range of primate taxa, with a focus on Malagasy lemurs [Godfrey et al., 2002; King et al., 2001; Schwartz et al., 2002]. In a synthesis testing a number of hypotheses concerning variation in primate dental development, Godfrey et al.  found that folivores did exhibit accelerated development by the age at weaning. They suggested that dietary hypotheses based on foraging independence and food processing explain developmental variation better than those that connect dental development to life history or its correlates. While they did not examine dental development beyond the age at weaning, the results of this study support their food-processing hypothesis, which suggests that selection has acted on these animals’ ability to process a folivorous diet by accelerating dental development [Godfrey et al., 2001]. Because of the small sample size, limited comparisons, and degree of intraspecific variation in the current study, the results must be interpreted with caution. Nevertheless, it was found that, in comparison with less-folivorous species, the folivores initiated 38 / Dirks crown formation of the slowest-forming molar earlier, had a shorter period of crown formation, and experienced earlier emergence of the third molar. 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