Journal of Human Evolution 82 (2015) 137e144
Contents lists available at ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
Dental eruption in East African wild chimpanzees Zarin Machanda a, Nick F. Brazeau a, Andrew B. Bernard b, Ronan M. Donovan c, Amanda M. Papakyrikos d, Richard Wrangham a, Tanya M. Smith a, * a
Department of Human Evolutionary Biology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA Freelance Nature Photographer, 28 Fithian Avenue, Merchantville, NJ 08109, USA c Freelance Nature Photographer, 9063 Douglas Circle, Helena, MT 59602, USA d Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA 02481, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 July 2014 Accepted 10 February 2015 Available online 18 March 2015
Knowledge of chimpanzee development has played an essential role in our understanding of the evolution of human ontogeny. However, recent studies of wild ape dentitions have cast doubt on the use of developmental standards derived from captive individuals. Others have called into question the use of deceased wild individuals to infer normative development. We conducted a high resolution photographic study of living known-age subadults in the Kanyawara community (Kibale National Park, Uganda) to generate a comprehensive three year record of dental eruption (including tooth emergence ages). These non-invasive data allow comparisons of captive and wild chimpanzees, establish accurate developmental standards for relatively healthy wild individuals, and facilitate direct assessments of primate-wide associations between dental development and life history. Emergence ages in the Kanyawara chimpanzees are very similar to living Gombe chimpanzees, and are broadly comparable to deceased Taï Forest chimpanzees. Early-emerging teeth such as the deciduous dentition and first molar (M1) appear during a time of maternal dependence, and are almost indistinguishable from captive chimpanzee emergence ages, while later forming teeth in the Kanyawara population emerge in the latter half of captive age ranges or beyond. Five juveniles whose lower M1s emerged by or before 3.3 years of age continued to nurse for a year or more beyond M1 emergence, and their mothers showed considerable variation in reproductive rates. The third molars of two adolescent females emerged several months to several years prior to the birth of their first offspring. Given that broad primate-wide relationships between molar emergence and life history do not necessarily hold within this population of chimpanzees, particularly for variables that are reported to be coincident with molar emergence, we suggest that further study is required in order to predict life history variables in hominins or hominoids. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Tooth emergence Dental development Weaning Life history Human evolution
Introduction In humans and other primates, subadults are routinely aged by comparing tooth eruption1 patterns with those of known-aged individuals (Smith et al., 1994; Hillson, 2005; AlQahtani et al., 2010). Among chimpanzees, early studies of tooth development
* Corresponding author. E-mail address: [email protected] (T.M. Smith). 1 The terms ‘eruption’ and ‘emergence’ are defined here as follows: eruption is the process of tooth movement from within the alveolar crypt to the fully occluded position in the dental arcade, while emergence refers to the event within the eruptive process whereby the tooth first becomes visible at the margins of the jaw bone (alveolar emergence) or gumline (gingival emergence). Here we use the term ‘emergence’ to refer to gingival emergence unless otherwise specified. http://dx.doi.org/10.1016/j.jhevol.2015.02.010 0047-2484/© 2015 Elsevier Ltd. All rights reserved.
reported emergence ages for small numbers of captive animals or museum specimens (reviewed in Smith et al., 2007). This includes a longitudinal study by Nissen and Riesen, who presented the first data on gingival (gumline) emergence in several individuals of known age (Nissen and Riesen, 1945, 1964). In 1945, they reported emergence ages for the deciduous (primary) dentition of 16 captive individuals, followed by a 1964 report on the emergence of the permanent dentition of 15 of the original 16 chimpanzees. Subsequently Conroy and Mahoney (1991) conducted intraoral exams of 58 known-age captive chimpanzees in a ‘mixed’ longitudinal study (enrolling different-aged subadults who were followed for one to nine years), yielding a somewhat larger data set on deciduous and permanent emergence ages in captive individuals (also see Kuykendall et al., 1992). These data have been used as the basis for comparisons with fossil hominins, leading to the hypothesis that
138
Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144
Plio-Pleistocene hominins possessed an ape-like growth pattern, as first molar emergence ages were estimated to be very similar to those of captive chimpanzees (Bromage and Dean, 1985; Smith, 1986; Smith and Tompkins, 1995; Anemone et al., 1996). Recent studies have called into question the appropriateness of developmental data derived from captive animals for the reconstruction of hominin life history (Zihlman et al., 2004, 2007; Kelley and Schwartz, 2010, 2012). Zihlman et al. (2004) estimated maxillary emergence ages from dry skulls of West African wild chimpanzees (Pan troglodytes verus), which appeared to show later ages than captive individuals. However, Smith et al. (2010) reassessed the Taï Forest chimpanzee skeletons and found that ages at death in half of the subadults employed by Zihlman et al. (2004) were not known with accuracy sufficient for precise comparisons with captive chimpanzees. Moreover, one key individual in the former study was misidentified during field recovery, leading to overestimated ages for incisor and second molar emergence. Smith et al. (2010) concluded that emergence ages in two remaining knownaged Taï individuals appear to fall near the middle or latter half of captive emergence ranges, which does not support the “unambiguous pattern” of slower wild chimpanzee tooth formation reported by Zihlman et al. (2004:10541). Smith and Boesch (2011) extended these results to suggest that an important source of developmental variation may be the use of deceased wild individuals, who are more likely to have experienced developmental delay due to stress or pathology. They concluded that tooth emergence ages must be established from living individuals. Here we present the ages of dental emergence of the deciduous and permanent dentition of East African wild chimpanzees (Pan troglodytes schweinfurthii) determined for known-age living subadults from the Kanyawara community in Kibale National Park, Uganda. Tooth eruption stages (absence, initial emergence/first appearance, partial emergence, full occlusion), as well as the duration of eruption from the gumline to the occlusal plane, were assessed from a multitude of high-resolution photographs taken over 39 months. We also provide updated information for our initial assessment of first molar (M1) emergence and life history variables (Smith et al., 2013), including new ages at weaning, resumption of sexual swelling, subsequent pregnancy, and interbirth intervals for multiparous mothers. These data provide important insight into developmental variation within a species, facilitating comparisons with large samples of captive individuals, as well as a few known-aged wild chimpanzees. Knowledge of wild chimpanzee dental development is also important for assessing the age of unknown individuals, including subadult females who routinely immigrate into new communities. Finally, these new developmental standards represent an important comparative sample for the study of juvenile fossil hominins.
Table 1 Kanyawara wild chimpanzees included in this study. Name WZ (Winza) MM (Mango) OB (Tembo) RB (Burma) TR (Thatcher) UK (Buke) LE (Betty) BT (Basuta) AN (Azania) OL (Gola) MN (Moon) WC (Wallace) QV (Quiver) WE (Wenka) OM (Omusisa) TS (Tsunami) AZ (Likizo) UN (Unasema) EU (Euro) BO (Bono) OG (Tacugama) TT (Tuber) NP (Special) AT (Tuke) OT (Tenkere) MX (Max) PB (Bud)
Sex
Birth date
First photo age (yrs)
Last photo age (yrs)
M F M M F F F M F F M M M F F F M M F M M M F M F M M
5/25/2012 1/21/2012 1/20/2012 11/17/2011 11/12/2011 4/6/2011 1/2/2011 6/23/2010 5/1/2009 3/3/2009 12/26/2008 8/5/2008 8/3/2008 6/22/2007 6/23/2005 1/23/2005 12/28/2004 11/1/2004 5/25/2004 10/22/2003 4/10/2001 11/1/2000 2/9/2000 11/2/1999 2/13/1999 1/15/1998 1/20/1995
0.4 0.5 0.3 0.6 0.4 0.2 0.7 1.2 2.5 2.5 2.6 3.1 2.8 4.3 5.9 6.6 6.4 7.1 7.2 7.9 9.9 10.4 11.6 11.5 13.6 13.4 16.3
1.4 2.3 2.4 0.8 2.5 2.9 1.9 3.9 4.9 3.6 5.4 5.8 4.3 5.4 7.3 9.0 9.4 9.2 e 10.6 13.2a 13.1a 14.3a 14.6a 15.7a 14.2b 19.4a,b
a
All teeth erupted prior to the end of photographic recording. Third molar teeth erupted later than in other individuals possibly due to tooth impaction. b
absence of teeth. Tooth emergence was assessed from exposed cusp tips at or just above the gumline, which is the standard used in laboratory settings and for living humans. When possible we used subsequent images to confirm that small protein stained regions of postcanine tooth crowns were closely followed by the emergence of the mesial and distal aspects of the crown. We chose not to extrapolate ages when initial emergence was not captured in photographs, thus the only error associated with our emergence
Methods Several dedicated photographers (RMD, ABB, and NFB) accompanied a team of field assistants to locate and photograph subadult chimpanzees from the Kanyawara community in Kibale National Park (Uganda) from March 2011 through June 2014. The Kanyawara community consisted of 53e54 habituated individuals during this time, including more than 25 subadults aged 0e15 years whose births are known to within a month or less (Table 1). Photographic data on dental eruption were collected when chimpanzees were resting, grooming, or playing (Fig. 1). High-resolution photographs were taken using a digital SLR camera with high ISO capability (at least 3200), high frames per second (at least six), and a wide aperture lens (f/4 at 200 mm). Approximately 2,500 photographs of subadult community members taken on a weekly or monthly basis were examined by AP and TMS for information on the presence or
Figure 1. Deciduous tooth emergence in a two-month old wild chimpanzee female infant. The image depicts Buke at approximately 58 days of age showing initial emergence of her deciduous lower central incisors and deciduous third premolars (small white spots in the pink U-shaped dental arcade). Her deciduous lower lateral incisors appeared shortly before 93 days of age, the deciduous lower fourth premolars were first seen fully erupted at 315 days of age, and the deciduous lower canine appeared to cut the gum at 437 days of age. She was estimated to be three weeks old when she was first observed with her mother.
Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144
ages is due to uncertainty in date of birth (which was never more than one month, and often substantially less). Emergence ages were compared with wild and captive chimpanzees (Nissen and Riesen, 1945, 1964; Pusey, 1978; Conroy and Mahoney, 1991; Kuykendall et al., 1992; Smith et al., 2010), as well as living humans (Clements and Zuckerman, 1953; Garn et al., 1959; Demirjian and Levesque, 1980; Liversidge, 2003; Liversidge and Molleson, 2004; AlQahtani et al., 2010). Here we also report certain life history variables that Smith (1989) found to be positively correlated with molar emergence: age at weaning, interbirth interval (IBI), and age of first birth for females, as well as information on when mothers returned to regular sexual swelling cycles and dates of subsequent conceptions. Weaning is a process that encompasses transitions from 100% suckling to 100% solid food intake; events may include the initial incorporation of solid food, the resumption of maternal estrous cycling, or the cessation of suckling (Lee, 1996; Borries et al., 2014). Here we define weaning as the cessation of suckling. While the value of this measure is debatable, it is useful because it has been reported for various populations of chimpanzees and other great apes (discussed further in Smith et al., 2013). Interbirth intervals were calculated using completed birth intervals (i.e., those that conclude with a birth) where the birthdates of offspring were known to the month. Photographic and behavioral data collection protocols were approved by the Harvard University Faculty of Arts and Sciences Institutional Animal Care and Use Committee. Results The deciduous dentitions of five individuals were completely erupted by ~1.2e1.5 years of age, and tooth-specific emergence ages of eight individuals fell within captive ranges or earlier (Fig. 2). The typical emergence sequence was di1, di2, dp3, dp4, dc, although the di2s emerged prior to the di1s in one individual
139
(Mango). Deciduous teeth were shed between ~6.4 and 10.9 years of age in eight individuals (Table 2), and the deciduous canines were the last tooth type to be lost. Six individuals' lower M1s emerged by or before 3.3 years of age (Table 3; Fig. 3). Dental emergence in the complete permanent dentition largely fell within captive ranges (Table 4; Fig. 4). Male canine emergence may exceed captive ranges (male captive maximum ¼ 9.8e10.1 years [upper and lower canines, respectively], n ¼ 8 individuals; Nissen and Riesen, 1964); the canines of two males (Tacugama and Tuber) emerged later than 10.1 years of age, and the canines of a third individual (Bono) emerged at an age near the captive maximum (Fig. 5). Two individuals (Max and Bud) showed third molar (M3) emergence ages that exceeded captive ranges (captive maximum ¼ 13.1e13.6 years [lower and upper M3s, respectively], n ¼ 14 individuals; Nissen and Riesen, 1964), although one or both of these individuals' M3s may have been impacted, as several other individuals showed M3 emergence prior to 12 years of age. Upper M3s were the last tooth to erupt, and thus we consider normative dental maturity to be achieved between ~11 and 13 years of age in this community (save for the two individuals in whom tooth impaction may have delayed eruption). This sample included one known-age female in whom the upper M3s emerged prior to 11.6 years of age. Further study is required to determine if wild chimpanzee females reach dental maturity earlier than males. Overall, lower molar emergence (M1, M2, or M3) preceded upper molar emergence in six of the seven individuals for whom precise lower molar emergence ages could be determined. Although it was not possible to determine the precise age of upper M1 emergence, which occurred later than lower M1 emergence in at least three individuals, a delay of more than 0.5 years between lower and upper M1 emergence was apparent in two individuals (Azania and Moon). Similarly, a delay of more than one year was noted between the emergence of the lower and upper M2 of an older individual (Omusisa), and emergence of the upper M2s had
Figure 2. Lower deciduous tooth emergence in captive and wild chimpanzees. di1 ¼ deciduous central incisor, di2 ¼ deciduous lateral incisor, dc ¼ deciduous canine, dp3 ¼ deciduous third premolar, dp4 ¼ deciduous fourth premolar. Horizontal bars indicate captive emergence age ranges from Nissen and Riesen (1945) and Kuykendall et al. (1992). Wild Kanyawara chimpanzee data are indicated as ‘E’ for emerging, which is directly comparable to captive ranges. Additional individuals for which emergence was not directly observed are represented under horizontal captive bars by open circles for pre-emergent (unerupted) teeth, and closed circles for teeth that had already emerged through the gingiva. Kanyawara sample sizes range from five to seven individuals per tooth type; multiple observations are included for a few individuals when the tooth progressed from pre-emergent to emergent but gingival emergence was not observed directly.
140
Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144 Table 2 Ages of deciduous tooth loss (in years) in the Kanyawara wild chimpanzees. Tootha
Age (years)
Uid1
7.0 > 6.8 e < 7.3 > 7.0 e < 7.2 > 6.8 e < 7.3 > 7.8 e < 9.0 > 9.1 e < 10.0 < 9.9 < 10.4 > 7.7 e < 9.2 < 7.9 > 7.7 e < 9.2 < 7.9 6.4 > 6.8 e < 7.3 7.5 > 6.9 e < 7.2 > 7.8 e < 9.0 > 9.1 e < 10.1 10.6 > 10.6 e < 10.9 > 7.2 < 7.9 > 7.7 e < 9.2 > 9.0 e < 9.4 > 7.0 e < 7.3 > 7.2 < 7.9 > 7.7 e < 9.2 > 7.9 e < 8.9
Uid2 Udc
Udp3 Udp4 Ldi1 Ldi2 LdC
Ldp3
Ldp4
a U ¼ upper, L ¼ lower, di1 ¼ deciduous central incisor, di2 ¼ deciduous lateral incisor, dc ¼ deciduous canine, dp3 ¼ deciduous third premolar, dp4 ¼ deciduous fourth premolar. Each row represents a different individual for each tooth type from a total of eight individuals observed to have shed deciduous teeth.
Figure 3. First molar emergence in a 2.8 year-old wild chimpanzee female infant. The image depicts Buke at 2.8 years of age showing initial emergence of her lower first molars. The left M1 (on the right of the image) is slightly obscured by a light-colored food item, and both molars show small black particles near the tip of the mesiobuccal cusp. The left M1 may be slightly advanced relative to the right M1, and by 2.9 years of age the mesial cusps were completely erupted.
yet to occur more than 0.4e0.6 years after the lower M2s had emerged in three other individuals. Two individuals' upper M3s also emerged a year or more after their lower M3s (Tacugama and Tuber). One 16.3 year-old (Bud), who may have had impacted M3s, showed similar timing for initial emergence of the upper left and lower right M3s. However, the upper left M3 emerged several months earlier than the upper right counterpart, which remained in an atypical tilted physical position for over two years, lending further support to the possibility that one or more of his M3s were partially impacted. In one individual (Omusisa) it was possible to approximate the variation between the emergence of left and right teeth; her upper I1s emerged approximately 28 days apart, her lower I1s emerged more than 100 days apart, her upper I2s emerged 21 days apart, and her lower M2s came in 56 days apart. Finally, we estimated the duration of the eruption process in individuals for whom initial emergence and subsequent advancement could be observed
(Table 5). For example, the duration of lower M1 eruption from gingival emergence to the final occlusal position took 0.2e0.5 years in two individuals (Gola and Azania). Most canines took approximately one year to achieve full eruption, while the duration of eruption among all molars ranged from 0.2 to 1.1 years. Discussion Comparative perspectives on chimpanzee dental eruption This study represents the most comprehensive assessment of dental eruption in wild chimpanzees to date. Emergence ages for
Table 3 Kanyawara chimpanzee first molar emergence (in years) and life history information. Individual Sex
Birth
Bukea Azania Gola Moon Wallace
F F F M M
Quiver Wenka
M 8/3/2008 F 6/22/2007
a
4/6/2011 5/1/2009 3/3/2009 12/26/2008 8/5/2008
Lower M1 Upper M1
Weaning
Initial resumption of maternal swelling/pregnancy
2.8 3.0 3.5 3.8
Contents lists available at ScienceDirect
Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
Dental eruption in East African wild chimpanzees Zarin Machanda a, Nick F. Brazeau a, Andrew B. Bernard b, Ronan M. Donovan c, Amanda M. Papakyrikos d, Richard Wrangham a, Tanya M. Smith a, * a
Department of Human Evolutionary Biology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA Freelance Nature Photographer, 28 Fithian Avenue, Merchantville, NJ 08109, USA c Freelance Nature Photographer, 9063 Douglas Circle, Helena, MT 59602, USA d Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA 02481, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 July 2014 Accepted 10 February 2015 Available online 18 March 2015
Knowledge of chimpanzee development has played an essential role in our understanding of the evolution of human ontogeny. However, recent studies of wild ape dentitions have cast doubt on the use of developmental standards derived from captive individuals. Others have called into question the use of deceased wild individuals to infer normative development. We conducted a high resolution photographic study of living known-age subadults in the Kanyawara community (Kibale National Park, Uganda) to generate a comprehensive three year record of dental eruption (including tooth emergence ages). These non-invasive data allow comparisons of captive and wild chimpanzees, establish accurate developmental standards for relatively healthy wild individuals, and facilitate direct assessments of primate-wide associations between dental development and life history. Emergence ages in the Kanyawara chimpanzees are very similar to living Gombe chimpanzees, and are broadly comparable to deceased Taï Forest chimpanzees. Early-emerging teeth such as the deciduous dentition and first molar (M1) appear during a time of maternal dependence, and are almost indistinguishable from captive chimpanzee emergence ages, while later forming teeth in the Kanyawara population emerge in the latter half of captive age ranges or beyond. Five juveniles whose lower M1s emerged by or before 3.3 years of age continued to nurse for a year or more beyond M1 emergence, and their mothers showed considerable variation in reproductive rates. The third molars of two adolescent females emerged several months to several years prior to the birth of their first offspring. Given that broad primate-wide relationships between molar emergence and life history do not necessarily hold within this population of chimpanzees, particularly for variables that are reported to be coincident with molar emergence, we suggest that further study is required in order to predict life history variables in hominins or hominoids. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Tooth emergence Dental development Weaning Life history Human evolution
Introduction In humans and other primates, subadults are routinely aged by comparing tooth eruption1 patterns with those of known-aged individuals (Smith et al., 1994; Hillson, 2005; AlQahtani et al., 2010). Among chimpanzees, early studies of tooth development
* Corresponding author. E-mail address: [email protected] (T.M. Smith). 1 The terms ‘eruption’ and ‘emergence’ are defined here as follows: eruption is the process of tooth movement from within the alveolar crypt to the fully occluded position in the dental arcade, while emergence refers to the event within the eruptive process whereby the tooth first becomes visible at the margins of the jaw bone (alveolar emergence) or gumline (gingival emergence). Here we use the term ‘emergence’ to refer to gingival emergence unless otherwise specified. http://dx.doi.org/10.1016/j.jhevol.2015.02.010 0047-2484/© 2015 Elsevier Ltd. All rights reserved.
reported emergence ages for small numbers of captive animals or museum specimens (reviewed in Smith et al., 2007). This includes a longitudinal study by Nissen and Riesen, who presented the first data on gingival (gumline) emergence in several individuals of known age (Nissen and Riesen, 1945, 1964). In 1945, they reported emergence ages for the deciduous (primary) dentition of 16 captive individuals, followed by a 1964 report on the emergence of the permanent dentition of 15 of the original 16 chimpanzees. Subsequently Conroy and Mahoney (1991) conducted intraoral exams of 58 known-age captive chimpanzees in a ‘mixed’ longitudinal study (enrolling different-aged subadults who were followed for one to nine years), yielding a somewhat larger data set on deciduous and permanent emergence ages in captive individuals (also see Kuykendall et al., 1992). These data have been used as the basis for comparisons with fossil hominins, leading to the hypothesis that
138
Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144
Plio-Pleistocene hominins possessed an ape-like growth pattern, as first molar emergence ages were estimated to be very similar to those of captive chimpanzees (Bromage and Dean, 1985; Smith, 1986; Smith and Tompkins, 1995; Anemone et al., 1996). Recent studies have called into question the appropriateness of developmental data derived from captive animals for the reconstruction of hominin life history (Zihlman et al., 2004, 2007; Kelley and Schwartz, 2010, 2012). Zihlman et al. (2004) estimated maxillary emergence ages from dry skulls of West African wild chimpanzees (Pan troglodytes verus), which appeared to show later ages than captive individuals. However, Smith et al. (2010) reassessed the Taï Forest chimpanzee skeletons and found that ages at death in half of the subadults employed by Zihlman et al. (2004) were not known with accuracy sufficient for precise comparisons with captive chimpanzees. Moreover, one key individual in the former study was misidentified during field recovery, leading to overestimated ages for incisor and second molar emergence. Smith et al. (2010) concluded that emergence ages in two remaining knownaged Taï individuals appear to fall near the middle or latter half of captive emergence ranges, which does not support the “unambiguous pattern” of slower wild chimpanzee tooth formation reported by Zihlman et al. (2004:10541). Smith and Boesch (2011) extended these results to suggest that an important source of developmental variation may be the use of deceased wild individuals, who are more likely to have experienced developmental delay due to stress or pathology. They concluded that tooth emergence ages must be established from living individuals. Here we present the ages of dental emergence of the deciduous and permanent dentition of East African wild chimpanzees (Pan troglodytes schweinfurthii) determined for known-age living subadults from the Kanyawara community in Kibale National Park, Uganda. Tooth eruption stages (absence, initial emergence/first appearance, partial emergence, full occlusion), as well as the duration of eruption from the gumline to the occlusal plane, were assessed from a multitude of high-resolution photographs taken over 39 months. We also provide updated information for our initial assessment of first molar (M1) emergence and life history variables (Smith et al., 2013), including new ages at weaning, resumption of sexual swelling, subsequent pregnancy, and interbirth intervals for multiparous mothers. These data provide important insight into developmental variation within a species, facilitating comparisons with large samples of captive individuals, as well as a few known-aged wild chimpanzees. Knowledge of wild chimpanzee dental development is also important for assessing the age of unknown individuals, including subadult females who routinely immigrate into new communities. Finally, these new developmental standards represent an important comparative sample for the study of juvenile fossil hominins.
Table 1 Kanyawara wild chimpanzees included in this study. Name WZ (Winza) MM (Mango) OB (Tembo) RB (Burma) TR (Thatcher) UK (Buke) LE (Betty) BT (Basuta) AN (Azania) OL (Gola) MN (Moon) WC (Wallace) QV (Quiver) WE (Wenka) OM (Omusisa) TS (Tsunami) AZ (Likizo) UN (Unasema) EU (Euro) BO (Bono) OG (Tacugama) TT (Tuber) NP (Special) AT (Tuke) OT (Tenkere) MX (Max) PB (Bud)
Sex
Birth date
First photo age (yrs)
Last photo age (yrs)
M F M M F F F M F F M M M F F F M M F M M M F M F M M
5/25/2012 1/21/2012 1/20/2012 11/17/2011 11/12/2011 4/6/2011 1/2/2011 6/23/2010 5/1/2009 3/3/2009 12/26/2008 8/5/2008 8/3/2008 6/22/2007 6/23/2005 1/23/2005 12/28/2004 11/1/2004 5/25/2004 10/22/2003 4/10/2001 11/1/2000 2/9/2000 11/2/1999 2/13/1999 1/15/1998 1/20/1995
0.4 0.5 0.3 0.6 0.4 0.2 0.7 1.2 2.5 2.5 2.6 3.1 2.8 4.3 5.9 6.6 6.4 7.1 7.2 7.9 9.9 10.4 11.6 11.5 13.6 13.4 16.3
1.4 2.3 2.4 0.8 2.5 2.9 1.9 3.9 4.9 3.6 5.4 5.8 4.3 5.4 7.3 9.0 9.4 9.2 e 10.6 13.2a 13.1a 14.3a 14.6a 15.7a 14.2b 19.4a,b
a
All teeth erupted prior to the end of photographic recording. Third molar teeth erupted later than in other individuals possibly due to tooth impaction. b
absence of teeth. Tooth emergence was assessed from exposed cusp tips at or just above the gumline, which is the standard used in laboratory settings and for living humans. When possible we used subsequent images to confirm that small protein stained regions of postcanine tooth crowns were closely followed by the emergence of the mesial and distal aspects of the crown. We chose not to extrapolate ages when initial emergence was not captured in photographs, thus the only error associated with our emergence
Methods Several dedicated photographers (RMD, ABB, and NFB) accompanied a team of field assistants to locate and photograph subadult chimpanzees from the Kanyawara community in Kibale National Park (Uganda) from March 2011 through June 2014. The Kanyawara community consisted of 53e54 habituated individuals during this time, including more than 25 subadults aged 0e15 years whose births are known to within a month or less (Table 1). Photographic data on dental eruption were collected when chimpanzees were resting, grooming, or playing (Fig. 1). High-resolution photographs were taken using a digital SLR camera with high ISO capability (at least 3200), high frames per second (at least six), and a wide aperture lens (f/4 at 200 mm). Approximately 2,500 photographs of subadult community members taken on a weekly or monthly basis were examined by AP and TMS for information on the presence or
Figure 1. Deciduous tooth emergence in a two-month old wild chimpanzee female infant. The image depicts Buke at approximately 58 days of age showing initial emergence of her deciduous lower central incisors and deciduous third premolars (small white spots in the pink U-shaped dental arcade). Her deciduous lower lateral incisors appeared shortly before 93 days of age, the deciduous lower fourth premolars were first seen fully erupted at 315 days of age, and the deciduous lower canine appeared to cut the gum at 437 days of age. She was estimated to be three weeks old when she was first observed with her mother.
Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144
ages is due to uncertainty in date of birth (which was never more than one month, and often substantially less). Emergence ages were compared with wild and captive chimpanzees (Nissen and Riesen, 1945, 1964; Pusey, 1978; Conroy and Mahoney, 1991; Kuykendall et al., 1992; Smith et al., 2010), as well as living humans (Clements and Zuckerman, 1953; Garn et al., 1959; Demirjian and Levesque, 1980; Liversidge, 2003; Liversidge and Molleson, 2004; AlQahtani et al., 2010). Here we also report certain life history variables that Smith (1989) found to be positively correlated with molar emergence: age at weaning, interbirth interval (IBI), and age of first birth for females, as well as information on when mothers returned to regular sexual swelling cycles and dates of subsequent conceptions. Weaning is a process that encompasses transitions from 100% suckling to 100% solid food intake; events may include the initial incorporation of solid food, the resumption of maternal estrous cycling, or the cessation of suckling (Lee, 1996; Borries et al., 2014). Here we define weaning as the cessation of suckling. While the value of this measure is debatable, it is useful because it has been reported for various populations of chimpanzees and other great apes (discussed further in Smith et al., 2013). Interbirth intervals were calculated using completed birth intervals (i.e., those that conclude with a birth) where the birthdates of offspring were known to the month. Photographic and behavioral data collection protocols were approved by the Harvard University Faculty of Arts and Sciences Institutional Animal Care and Use Committee. Results The deciduous dentitions of five individuals were completely erupted by ~1.2e1.5 years of age, and tooth-specific emergence ages of eight individuals fell within captive ranges or earlier (Fig. 2). The typical emergence sequence was di1, di2, dp3, dp4, dc, although the di2s emerged prior to the di1s in one individual
139
(Mango). Deciduous teeth were shed between ~6.4 and 10.9 years of age in eight individuals (Table 2), and the deciduous canines were the last tooth type to be lost. Six individuals' lower M1s emerged by or before 3.3 years of age (Table 3; Fig. 3). Dental emergence in the complete permanent dentition largely fell within captive ranges (Table 4; Fig. 4). Male canine emergence may exceed captive ranges (male captive maximum ¼ 9.8e10.1 years [upper and lower canines, respectively], n ¼ 8 individuals; Nissen and Riesen, 1964); the canines of two males (Tacugama and Tuber) emerged later than 10.1 years of age, and the canines of a third individual (Bono) emerged at an age near the captive maximum (Fig. 5). Two individuals (Max and Bud) showed third molar (M3) emergence ages that exceeded captive ranges (captive maximum ¼ 13.1e13.6 years [lower and upper M3s, respectively], n ¼ 14 individuals; Nissen and Riesen, 1964), although one or both of these individuals' M3s may have been impacted, as several other individuals showed M3 emergence prior to 12 years of age. Upper M3s were the last tooth to erupt, and thus we consider normative dental maturity to be achieved between ~11 and 13 years of age in this community (save for the two individuals in whom tooth impaction may have delayed eruption). This sample included one known-age female in whom the upper M3s emerged prior to 11.6 years of age. Further study is required to determine if wild chimpanzee females reach dental maturity earlier than males. Overall, lower molar emergence (M1, M2, or M3) preceded upper molar emergence in six of the seven individuals for whom precise lower molar emergence ages could be determined. Although it was not possible to determine the precise age of upper M1 emergence, which occurred later than lower M1 emergence in at least three individuals, a delay of more than 0.5 years between lower and upper M1 emergence was apparent in two individuals (Azania and Moon). Similarly, a delay of more than one year was noted between the emergence of the lower and upper M2 of an older individual (Omusisa), and emergence of the upper M2s had
Figure 2. Lower deciduous tooth emergence in captive and wild chimpanzees. di1 ¼ deciduous central incisor, di2 ¼ deciduous lateral incisor, dc ¼ deciduous canine, dp3 ¼ deciduous third premolar, dp4 ¼ deciduous fourth premolar. Horizontal bars indicate captive emergence age ranges from Nissen and Riesen (1945) and Kuykendall et al. (1992). Wild Kanyawara chimpanzee data are indicated as ‘E’ for emerging, which is directly comparable to captive ranges. Additional individuals for which emergence was not directly observed are represented under horizontal captive bars by open circles for pre-emergent (unerupted) teeth, and closed circles for teeth that had already emerged through the gingiva. Kanyawara sample sizes range from five to seven individuals per tooth type; multiple observations are included for a few individuals when the tooth progressed from pre-emergent to emergent but gingival emergence was not observed directly.
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Z. Machanda et al. / Journal of Human Evolution 82 (2015) 137e144 Table 2 Ages of deciduous tooth loss (in years) in the Kanyawara wild chimpanzees. Tootha
Age (years)
Uid1
7.0 > 6.8 e < 7.3 > 7.0 e < 7.2 > 6.8 e < 7.3 > 7.8 e < 9.0 > 9.1 e < 10.0 < 9.9 < 10.4 > 7.7 e < 9.2 < 7.9 > 7.7 e < 9.2 < 7.9 6.4 > 6.8 e < 7.3 7.5 > 6.9 e < 7.2 > 7.8 e < 9.0 > 9.1 e < 10.1 10.6 > 10.6 e < 10.9 > 7.2 < 7.9 > 7.7 e < 9.2 > 9.0 e < 9.4 > 7.0 e < 7.3 > 7.2 < 7.9 > 7.7 e < 9.2 > 7.9 e < 8.9
Uid2 Udc
Udp3 Udp4 Ldi1 Ldi2 LdC
Ldp3
Ldp4
a U ¼ upper, L ¼ lower, di1 ¼ deciduous central incisor, di2 ¼ deciduous lateral incisor, dc ¼ deciduous canine, dp3 ¼ deciduous third premolar, dp4 ¼ deciduous fourth premolar. Each row represents a different individual for each tooth type from a total of eight individuals observed to have shed deciduous teeth.
Figure 3. First molar emergence in a 2.8 year-old wild chimpanzee female infant. The image depicts Buke at 2.8 years of age showing initial emergence of her lower first molars. The left M1 (on the right of the image) is slightly obscured by a light-colored food item, and both molars show small black particles near the tip of the mesiobuccal cusp. The left M1 may be slightly advanced relative to the right M1, and by 2.9 years of age the mesial cusps were completely erupted.
yet to occur more than 0.4e0.6 years after the lower M2s had emerged in three other individuals. Two individuals' upper M3s also emerged a year or more after their lower M3s (Tacugama and Tuber). One 16.3 year-old (Bud), who may have had impacted M3s, showed similar timing for initial emergence of the upper left and lower right M3s. However, the upper left M3 emerged several months earlier than the upper right counterpart, which remained in an atypical tilted physical position for over two years, lending further support to the possibility that one or more of his M3s were partially impacted. In one individual (Omusisa) it was possible to approximate the variation between the emergence of left and right teeth; her upper I1s emerged approximately 28 days apart, her lower I1s emerged more than 100 days apart, her upper I2s emerged 21 days apart, and her lower M2s came in 56 days apart. Finally, we estimated the duration of the eruption process in individuals for whom initial emergence and subsequent advancement could be observed
(Table 5). For example, the duration of lower M1 eruption from gingival emergence to the final occlusal position took 0.2e0.5 years in two individuals (Gola and Azania). Most canines took approximately one year to achieve full eruption, while the duration of eruption among all molars ranged from 0.2 to 1.1 years. Discussion Comparative perspectives on chimpanzee dental eruption This study represents the most comprehensive assessment of dental eruption in wild chimpanzees to date. Emergence ages for
Table 3 Kanyawara chimpanzee first molar emergence (in years) and life history information. Individual Sex
Birth
Bukea Azania Gola Moon Wallace
F F F M M
Quiver Wenka
M 8/3/2008 F 6/22/2007
a
4/6/2011 5/1/2009 3/3/2009 12/26/2008 8/5/2008
Lower M1 Upper M1
Weaning
Initial resumption of maternal swelling/pregnancy
2.8 3.0 3.5 3.8
