Cyclical nursing patterns in wild orangutans

Abstract

Nursing behavior is notoriously difficult to study in arboreal primates, particularly when offspring suckle inconspicuously in nests. Orangutans have the most prolonged nursing period of any mammal, with the cessation of suckling (weaning) estimated to occur at 6 to 8 years of age in the wild. Milk consumption is hypothesized to be relatively constant over this period, but direct evidence is limited. We previously demonstrated that trace element analysis of bioavailable elements from milk, such as barium, provides accurate estimates of early-life diet transitions and developmental stress when coupled with growth lines in the teeth of humans and nonhuman primates. We provide the first detailed nursing histories of wild, unprovisioned orangutans (Pongo abelii and Pongo pygmaeus) using chemical and histological analyses. Laser ablation inductively coupled plasma mass spectrometry was used to determine barium distributions across the teeth of four wild-shot individuals aged from postnatal biological rhythms. Barium levels rose during the first year of life in all individuals and began to decline shortly after, consistent with behavioral observations of intensive nursing followed by solid food supplementation. Subsequent barium levels show large sustained fluctuations on an approximately annual basis. These patterns appear to be due to cycles of varying milk consumption, continuing until death in an 8.8-year-old Sumatran individual. A female Bornean orangutan ceased suckling at 8.1 years of age. These individuals exceed the maximum weaning age reported for any nonhuman primate. Orangutan nursing may reflect cycles of infant demand that relate to fluctuating resource availability.

Keywords: Seasonality; barium; life history; non-human primates; nursing; orangutan; weaning.

Fig. 1. Temporal map and barium distribution in the first molar of an immature wild Bornean orangutan.

(A) Light microscopy image (left) of the mesiolingual cusp of the developing upper first molar (MCZ 5290) contrasted with an elemental map of the same section (right) showing the distribution of barium in the crown and root. Numbers on the microscopic image represent the age in days. High barium values in the outer enamel (red fringe) represent postdepositional modification of the subsurface enamel. Note that a small section of the subsurface root dentine was lost during preparation for elemental mapping [indicated by “*” here and in (B)]. (B) Calcium-normalized barium concentrations quantified in the dentine just below the enamel/root surface from the beginning of calcification (dentine horn tip below the enamel cusp) until death at 4.5 years of age (root tip). The approximate age of barium incorporation during dentine mineralization was determined from concurrently forming accentuated lines mapped with light microscopy (A). These ages are presented on a nonlinear scale that relates to the changing rate of extension during molar crown formation. The red bracket denotes a pattern of increasing barium incorporation due to milk consumption during the first year of life. Approximately annual marked decreases in barium/calcium begin around 400 days and continue until death, likely reflecting cycles of increased solid food consumption and reduced milk intake.

Fig. 2. Dentine barium patterns across the first molars of three immature wild orangutans.

Calcium-normalized barium concentrations quantified from the beginning of first molar calcification (dentine horn tip) until the end of crown formation or the end of available root dentine in three immature wild orangutans. Ages are presented on a nonlinear scale that relates to the changing rate of extension during molar crown formation. Red brackets denote an increasing pattern of barium incorporation due to milk consumption during the first 1 to 1.5 years of life. (A) Bornean individual (ZSM 1981/48), (B) Sumatran individual (ZSM 1981/246), and (C) Sumatran individual (ZMB 83508). Although barium concentrations were markedly different between animals, values were consistent among teeth from the same individual (see Figs. 3 and 4 and fig. S1). Interindividual variation is consistent with variation in barium breast milk from six modern human subjects (39).

Fig. 3. Barium distribution across three molars from an 8.4-year-old female Bornean orangutan (ZSM 1981/48).

Calcium-normalized barium concentrations quantified from the beginning of calcification (near the dentine horn tip) in the first molar (M1) until the cessation of third molar (M3) crown formation at death. Ages are presented on a nonlinear scale that relates to the changing rate of extension during molar crown formation. Absolute barium values found here are greater than for the other individuals in this study, as is the case for strontium, although calcium and other trace element values are comparable to other individuals. Solid arrows show the barium pattern used to register the concurrently forming M1 and M2, and dashed arrows show the M2 to M3 registry, which allowed the age at death to be determined from counts and measurements of incremental features. Complete cessation of suckling appears to have occurred just after a prolonged enrichment of barium concentration that ended at 8.1 years, which is apparent as a deep blue band in the last-formed dentine of the M2 and M3 (indicated by “*”). The M3 concentration plot shows this event, whereas the M2 plot does not because of the missing root tip.

Fig. 4. Barium distribution across three molars from an 8.8-year-old Sumatran orangutan (ZMB 83508).

Calcium-normalized barium concentrations quantified from the beginning of calcification in the first molar (M1) until the cessation of third molar (M3) crown formation at death. Ages are presented on a nonlinear scale that relates to the changing rate of extension during molar crown formation. Solid arrows show the barium pattern used to register the concurrently forming M1 and M2, and dashed arrows show the M2 to M3 registry, which allowed the age at death to be determined from counts and measurements of incremental features. A prolonged period of barium enrichment occurred just before death at 8.8 years, which is apparent as a green band in the last-formed dentine of the M3 and as elevated values in the M3 barium concentration plot (indicated by “*”). The histological map of this individual is given in fig. S2.

Fig. 5. Fruit availability (above) and average energetic intake (below) of four lactating wild Bornean orangutan females over 7 years.

Data are from the Tuanan Orangutan Research Area, Central Kalimantan, Indonesia [detailed by Vogel et al. (22, 51)]. Top: The percentage of fruiting trees derives from 1868 marked trees in monthly monitored phenology plots, 98% of which are species consumed by orangutans. Bottom: Mean daily caloric intake for four adult mother orangutans with nursing offspring (ranging from 0 to 6 years in age) collected from 2003 to 2010. Data are based on 12,669 hours from 1100 full-day focal animal follows.