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 
 
 Our method complements dietary studies of wild primates that produce temporally restricted measures of isotopes or trace elements from samples of hair or feces [reviewed by Tsutaya and Yoneda ( 15 )]. Trace element analyses of teeth can be anchored to incremental growth lines to assign ages to specific values, yielding a precise longitudinal perspective that begins before birth and may continue until death ( 10 , 16 ). Here, we show that accurate nursing histories and weaning ages can be determined from primate dentitions in zoological museums that were collected many decades ago. This approach is especially timely for critically endangered taxa, such as Sumatran and Bornean orangutans, Pongo abelii and Pongo pygmaeus, whose slow rate of growth and reproduction is a significant liability in a region that is being rapidly deforested. 
 
 Nursing infants rapidly incorporate barium from milk into their skeletal tissues, including bones and teeth ( 10 ), as is the case for calcium and lead ( 13 , 14 ). Thus, barium passes from one generation to the next, because stores originally incorporated into skeletal tissues during the mother’s development are mobilized for her infant. Minor contributions may also come from dietary sources, air, and water; however, most of the barium that is not incorporated into skeletal tissues is excreted within 1 to 2 weeks ( 12 ). Macaque mothers on a uniform diet show differences in barium levels in their milk ( 10 ), representing additional evidence that barium concentrations are primarily a function of somatic stores rather than dietary sources of barium. Therefore, elevated barium values in the teeth of nursing infants and immature individuals reflect the ingestion of maternal milk rather than nonmilk foods consumed directly or by their mothers while nursing. 
 
 During lactation, mammals produce calcium-rich milk by drawing on skeletal reserves. Approximately 99% of the calcium in the body is found in bone, and the remaining amount in blood and organ tissues is continuously adjusted to maintain homeostasis. Certain low-level nonessential elements, such as barium and lead, often follow the movement of calcium in the body because they share certain transport pathways. These elements are preferentially concentrated in mothers’ milk, although barium passes through a partial filtering system (biopurification), making it proportionately less common than calcium. We have recently detailed an approach to document nursing in primates that integrates elemental mapping of barium concentrations and developmental analysis of teeth ( 10 ). Barium is an accurate indicator of milk provisioning because of the shared chemical properties with calcium, and it is more readily absorbed from maternal milk than from other dietary items ( 10 , 11 ). For example, barium sulfate is used as a contrast agent for x-ray imaging because very little is absorbed by the gastrointestinal tract ( 12 ). 
 
 Life history, or the way in which organisms allocate energy to growth, reproduction, and maintenance, is fundamental to a species’ biology and behavior. Lactation is a significant energetic investment for mammalian mothers, whose reproductive success is also affected by environmental conditions ( 1 ). Orangutans live in highly variable and unpredictable environments and have lower daily energy expenditures when compared with humans and other mammals ( 2 , 3 ). This strategy of energy minimization has been hypothesized to facilitate the avoidance of starvation during episodes of fruit scarcity in these large-bodied primates, resulting in the slowest life histories of any nonhuman primate ( 2 , 4 , 5 ). However, little is known about weaning age in wild orangutans, nor other aspects of life history, such as life span. Experienced field biologists have concluded that observational approaches do not permit comprehensive quantification of suckling duration or milk intake in wild orangutans and other arboreal primates ( 6 ). Infants and older immature individuals may suckle inconspicuously, as well as while nesting with mothers at night, both difficult to detect in an arboreal environment ( 7 ). Moreover, continuous long-term field studies encounter obstacles while documenting a process that may last for seven or more years, and they typically rely on age estimations because exact birth dates are rarely known ( 4 , 8 , 9 ). 
 
 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. 
 
 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. 
 
 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 ). 
 
 ( 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. 
 
 Histological and elemental maps of the molars of four immature orangutans reveal an increase in barium values throughout the first year of life ( Figs. 1 and 2 ). After the first year, the four immature orangutans in our study show episodic decreases in barium concentrations on an approximately yearly basis ( Figs. 1 , 3 , and 4 and fig. S1). Cyclical patterns of barium levels persist into the eighth year of life in a Bornean female and into the ninth year of life in a Sumatran male and a second Sumatran individual of unknown sex. One Bornean female shows a sustained decrease in barium concentrations below baseline levels around 8.1 years of age, suggesting complete cessation of suckling before her death at 8.4 years of age ( Fig. 3 ). Our oldest individual, an 8.8-year-old Sumatran individual of unknown sex, shows a broad elevated barium band for several months before its death ( Fig. 4 ). Thus, at this age, it does not appear to have ceased suckling. 
 
 DISCUSSION 
 
 Nursing patterns during the first year of life All four orangutans show a gradual increase in barium values from birth through their first year of life. Consistent with our findings, behavioral observations of wild Bornean orangutans report that they rely almost exclusively on mothers’ milk in their first year; solid food supplementation only becomes an appreciable component of their diet between 12 and 18 months of age (6, 9). A similar pattern of increasing barium concentration was found in the first molars of rhesus macaques in their first 3 months of life (10). The initially low milk volume in the neonatal period increases during exclusive milk feeding as a function of infant growth, increased gastric capacity, and expanded behavioral repertoire (17). After 3 months, the barium levels in macaque teeth decreased, coincident with the consumption of solid foods. Thus, the initial pattern of barium concentration slowly increasing, peaking, and declining in wild orangutans and captive macaques reflects the inverted U-shaped curve of primate lactation (18). 
 
 Nursing patterns after the first year of life We found that barium values decreased between 12 and 18 months of age in the four orangutans and then began to cycle on an approximately annual basis. This decreasing barium signature in teeth corresponds with the transition from a predominant milk diet to one characterized by increasing intake of solid foods. In contrast to seasonally breeding primates, such as rhesus macaques, orangutan females nurse their offspring over multiple years, enduring extreme and unpredictable inter- and intra-annual fluctuations in fruit availability (Fig. 5) (5, 9, 19–22). Cyclical episodes of decreased barium concentrations in immature orangutans likely reflect elevated solid food consumption during periods of high fruit availability. Confirmation of this hypothesis will require behavioral data from individuals whose barium concentrations may be quantified concurrently. This is a particular challenge because most museum specimens, including those in the current study, were collected long before primatological field sites were established in Indonesia and Malaysia (23). Periods of increased fruit availability not only alleviate infant demand of maternal resources but also afford females the opportunity to replenish energetic reserves to sustain lactation and/or transition to their subsequent reproduction. 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. We interpret sustained cyclical increases in barium after the first year of life as periods of volumetric increases in milk consumption by infants when fruit or other preferred foods were limited. Immature orangutans may struggle to recognize or to process certain food items and will beg or attempt to scrounge maternal foods while nursing and possibly beyond the weaning process (6). Physiological studies of captive orangutans indicate that they experience an extreme form of low-energy throughput (2), and wild adult Bornean individuals are known to catabolize fat reserves and muscle tissue during periods of nutrient insufficiency (5, 24, 25). These physiological responses are hypothesized to be due to the extreme ecological unpredictability of Indonesian forests, which may be a particular challenge for immature individuals with limited fat reserves, muscle tissue, and foraging ability. Thus, the prolonged cyclical increases in barium concentration in our individuals’ dentitions are likely due to intensified reliance on their mothers’ milk—a rich source of bioavailable barium. This demand likely relaxes during periods of high fruit availability. More abbreviated increases in barium concentrations (discrete spikes in barium graphs and thin elevated bands in elemental maps) may denote periods of physiological stress where trace elements in the infant’s own skeletal stores are released into the bloodstream and incorporated into mineralizing teeth. Moderate to severe illnesses and periods of significant weight loss are correlated with rapid increases in barium concentrations in the teeth of recently weaned captive macaques (26). These short-lived increases in barium are distinct from the more gradual pattern seen during nursing. Indications of physiological stress are consistent with developmental disruptions in the dentitions of several of our individuals (27). Comparative studies of external defects (enamel hypoplasias) report higher frequencies in orangutans than in other great apes (28). Wild orangutans appear to experience early life stress routinely, at least during the decades when most zoological museums acquired specimens from Indonesian expeditions. The presence of developmental defects alone is insufficient to distinguish among causes, such as nutritional deficiencies, immune challenges, or social stress (29, 30). Although data on captive primates and human children with associated medical records have provided insight into the etiology of these defects [for example, (26, 29, 31)], these conclusions are more difficult for wild primates (30). Characterizations of structural defects and elemental incorporation coupled with behavioral and ecological data are needed to determine why immature orangutans show high proportions of developmental defects in their teeth. 
 
 Barium and primate diets Available evidence on barium and other nonessential elements that are typically found at low physiological levels indicates limited absorption by humans and other primates from nonmilk dietary sources. The primary naturally occurring forms of barium are not water-soluble; thus, barium levels in drinking water are negligible unless contaminated from industrial waste sites (12). Few studies have measured barium in food, and none could be found specific to plant-based foods or insects in the diets of Indonesian orangutans. Evidence of barium levels across different parts of plants (for example, leaf, root, fruit, and flower) is mixed; there is some evidence that mature leaves contain more barium than young leaves (32–34). Even in cases where barium levels are high in certain plants or plant parts, barium is not absorbed in amounts that would be toxic to consumers (12, 32, 35). Barium absorption has been linked to the efficiency of calcium absorption rather than concentration in the food item (36). Our previous study of macaques revealed that the transition to nonmilk foods was associated with a sharp decline in tooth barium levels (10), likely due to the low bioavailability of barium in most plant-based foods. Therefore, the marked cyclical increases in barium concentration in the teeth of orangutans are unlikely to result from their consumption of nonmilk foods. The idea that these increases are due to barium in maternal diets is even less likely because gastrointestinal absorption of barium is age-dependent. For example, human adults absorb one-third to one-half of the barium absorbed by infants and immature individuals (37). Barium is discriminated against in favor of calcium (38), causing the barium/calcium ratio to decrease during the mother’s low-level absorption from her diet, then during excretion into maternal milk, and finally during absorption from maternal milk by the offspring. Thus, changes in maternal dietary barium intake have less influence on the offspring’s tooth barium than on the mother’s serum levels. The magnitude and cyclicity of fluctuations in tooth barium concentrations are unlikely to be caused by elemental variation in maternal milk during lactation. Following the initial phase of milk production, barium remains relatively constant throughout the rest of lactation, as is the case for lead (13). Barium values in milk from six human mothers collected over 5 months did not differ significantly within mothers (39). Samples of milk from two macaque mothers show only fairly small changes over 4 months (10). The infants of these two mothers do not show perfectly parallel trends in milk barium and tooth barium; the latter is highest during the period when they are exclusively suckling, peaking before breast milk barium values. We interpret this as a volumetric effect. It is also unlikely that the barium content of maternal milk changes appreciably during periods when orangutan mothers rely on reserves, releasing energy stored in body fat and protein (24). Muscles, fat, and connective tissue contain only 1 to 2% of the somatic stores of barium found in humans (12). An appreciable release of barium from skeletal reserves has only been documented during acute illness or starvation in mammals, and only for a short duration in these cases (26). Orangutan mothers would seriously compromise their health by mobilizing skeletal reserves in this extreme way during recurring periods of decreased energy intake. Although the amount of variation in dietary barium intake by orangutan mothers is unknown, the available evidence suggests that it is the quantity of ingested milk that varies throughout nursing, leading to fluctuations in the barium incorporated in teeth. 

 Orangutans Nurse For a Record-Breaking Amount of Time Video courtesy Gunung Palung Orangutan Project. 
 
 The world's largest tree climbers, orangutans now have another superlative to their name: They nurse their young longer than any other primate, a new study says. 
 
 Surprising new research has revealed that the colorful great apes suckle for up to eight years, and in some cases longer. 
 
 Little is known about when the shaggy great apes wean in the wild, in part because they're so challenging to study—they spend most of their time aloft and out of sight. But knowing when juveniles strike out on their own is important for conservationists working to save them. (See "Orangutans Are More Like Us Than You Think.") 
 
 For the new research, Tanya Smith and colleagues developed a creative method for tracking how long orangutans nurse: Analyzing the levels of barium, a trace element, in young orangutans' teeth. Because barium absorbs into young orangutans' skeletons from their mother's milk, it can reveal how long an orangutan had been nursing. 
 
 View Images Orangutans (pictured, a mom and baby) can live up to 50 years in the wild. 
 
 Photograph by Erin Vogel 
 
 “This paper represents an exciting new method of determining weaning age from the teeth of wild primates,” says biological anthropologist Cheryl Knott, director of the Gunung Palang Orangutan Project in Indonesia's Gunung Palung National Park. 
 
 Teeth Tell the Tale 
 
 Two species of orangutan—whose name comes from the Malay word for "person of the forest"—swing from the trees in Sumatra and Borneo: The Sumatran orangutan, Pongo abelii, and the Bornean orangutan, Pongo pygmaeus. (Also see "Pictures: Saving Sumatra's Orangutans.") 
 
 Smith, a biological anthropologist at Griffith University, and team studied the teeth of four immature orangutans, two from Borneo and two from Sumatra. The animals had been shot during collecting expeditions many years ago, their bones then housed in museums. 
 
 By studying growth patterns and barium levels in the specimens' molars, the team determined the animals' barium levels decreased after one year of age, but that the element was still there nearly a decade later, according to the study, published this week in Science Advances. 
 
 For instance, one Bornean orangutan weaned at 8.1 years of age, and a Sumatran orangutan was still suckling at the staggering age of 8.8 years old when it died. Orangutans have their first offspring around 15 years of age and are believed to live up to 50 years in the wild. (See "10 of Our Favorite Orangutan Pictures.") 
 
 Tough Times 
 
 The teeth also showed cyclical periods of high and low barium concentrations that corresponded with fruit abundance: When fruit was plentiful, barium levels were lower. 
 
 That suggests that in times of scarcity, young orangutans may "fall back" on mom's milk to get them through, says Smith. 
 
 Saving Orangutans in Sumatra's Disappearing Rain Forests 
 
 “In the wild, it's difficult to know how much milk the juveniles are actually ingesting, and this new study indicates that they are still obtaining substantial milk during this period," adds Knott. (Read more about Knott's work on orangutans in her own words.) 
 
 The unpredictable environment is also likely why orangutans mature more slowly—there's rarely a surplus of food that could fuel rapid growth. Indeed, if the fruit supply were more reliable, it's likely orangutans would not nurse so long, she says. 
 
 Captive primates tend to mature more quickly than their wild counterparts, for instance, presumably because they eat consistently and nutritiously, Smith notes. 
 
 Steady Decline 
 
 Since they reproduce so slowly, orangutans are particularly vulnerable; deforestation for palm oil plantations has dwindled their numbers, and they are now critically endangered. (Read "Schoolkids Write Adorable Book About Orphaned Orangutan.") 
 
 The island of Borneo (map) has lost more than 50 percent of their orangutan population in the past 60 years, and in the past 20 years the species' habitat has decreased by at least 55 percent. On Sumatra (map), just under 15,000 remain, according to WWF. That's a drop from possibly 230,000 of the primates a century ago. 
 
 Smith and colleagues' study suggests there need to be more research into orangutan moms and babies, Knott adds. (See "6 Fierce Animal Moms That Go to Extremes For Their Young.") 

 Biomarkers in the teeth of wild orangutans indicate nursing patterns related to food fluctuations in their habitats, which can help guide understanding of breast-feeding evolution in humans, according to a study published today in Science Advances. This work was led by researchers in the Department of Environmental Medicine and Public Health at the Icahn School of Medicine at Mount Sinai and evolutionary biologists at Griffith University in Australia. 
 
 Breast-feeding is a critical aspect of human development, and the duration of exclusive nursing and timing of introducing solid food to the diet are also important determinants of health in human and other primate populations. Many aspects of nursing, however, remain poorly understood. Orangutan nursing habits have also been difficult to study due to challenges in observing this behavior in their natural environment. To work around these challenges, researchers reconstructed diet histories of wild orangutans by using their teeth as biomarkers. The growth patterns of teeth, which resemble tree rings, allows investigators to determine concentrations of the maternal elements in the infants' teeth over time, which yields information about their nursing and dietary patterns. 
 
 "Early-life dietary transitions reflect fundamental aspects of primate life, history, and evolution," said Christine Austin, PhD, a postdoctoral fellow in the Department of Environmental Medicine and Public Health and second study author. "By first studying nursing patterns of our primate cousins, we can apply these findings to future studies in humans. This method can be used to reconstruct the diet histories of contemporary humans in order to reliably and accurately study the relationship between infant diet and health outcomes in childhood or later life, as well as inform models of population growth." 
 
 In this study, the researchers examined levels of the element barium in teeth samples from deceased Sumatran and Bornean orangutans housed in zoological museums. Teeth analyses showed that the orangutans consumed maternal milk exclusively for their first year, as determined by a gradual increase in barium levels over the first 12 months. After the first year, the teeth indicated cycles that alternated between more and less milk consumption, which may occur until eight to nine years of age, a later weaning age than any other primate. 
 
 This cycling is believed to result from the changing and unpredictable availability of fruit, which leads young orangutans to rely on maternal milk for a longer period of time. "The evidence of cyclical multi-year nursing patterns and late weaning ages in orangutans, reported here for the first time, will lead to further studies of how food availability and other environmental factors affect nursing patterns in primates," said Tanya Smith, PhD, Associate Professor at Griffith University and lead study author. "Additional research is needed to determine whether similar breast-feeding patterns help human babies increase resilience to environmental stressors in infancy."
– Orangutans nurse their young for up to eight years or longer, a new study finds—a record for primates. As National Geographic notes, it's difficult to study orangutans in the wild since they're so often out of sight in trees, but it's important for conservationists to know when juveniles become independent. Orangutans reproduce for the first time around age 15 and are estimated to live up to 50 years in the wild. They reproduce slowly, the New York Times reports, with mothers raising one baby at a time for six to nine years before birthing another. To determine nursing length, researchers analyzed the levels of barium (a trace element that orangutans absorb from their mother's milk) in the teeth of four young orangutans whose bones had been kept in museums. The team found that one orangutan weaned at 8.1 years old; another was still nursing when it died at 8.8 years old. Before this research, scientists estimated orangutans might nurse for six to eight years, but it was difficult to know since field surveys are so challenging. Because the growth patterns of teeth "resemble tree rings" and can be easily dated, per a press release, they also revealed other interesting aspects of the nursing relationship: During periods of time when fruit was known to be abundant, barium levels were lower, and vice versa, indicating that when food was scarce, young orangutans nursed more. Researchers believe the fact that orangutans' food supply is unpredictable is part of the reason they nurse so long—captive primates with a steady supply of food tend to mature at a faster rate than wild primates. (Apes may be able to "read minds.")