Macronutrient composition of olive baboon (Papio anubis) milk: A comparison to rhesus macaque (Macaca mulatta) milk

Abstract

This study was designed to (1) characterize the macronutrient composition of olive baboon (Papio anubis) milk, (2) compare baboon milk composition to that of rhesus macaques (Macaca mulatta), and (3) evaluate the association between the proportion of milk energy derived from protein and relative growth rate within anthropoid primates. A single milk sample was collected from each of eight lactating olive baboons ranging between 47- and 129-days postparturition and six rhesus macaques from 15- to 92-days living at the same institution under identical management conditions. Macronutrient composition (water, fat, protein sugar, and ash) was determined using standard techniques developed at the Nutrition Laboratory at the Smithsonian National Zoological Park. Baboon milk on average contained 86.0% ± 0.6% water, 4.7% ± 0.5% fat, 1.6% ± 0.04% protein, 7.3% ± 0.07% sugar, and 0.165% ± 0.007% ash. Baboon milk gross energy (GE) averaged 0.81 ± 0.04 kcal/g with 51.9% ± 2.6% from fat, 11.8% ± 0.7% from protein, and 36.2% ± 2.0% from sugar. Baboon milk demonstrated strong similarity to milk composition of the closely phylogenetically related rhesus macaque (86.1% ± 0.3% water, 4.1% ± 0.4% fat, 1.69% ± 0.05% protein, 7.71% ± 0.08% sugar, 0.19% ± 0.01% ash, and 0.78 kcal/g). There was no statistical difference between baboon and macaque milk in the proportions of energy from fat, sugar, and protein. Baboon milk can be described as a high sugar, moderate fat, and low protein milk with moderate energy density, which is consistent with their lactation strategy characterized by frequent, on-demand nursing and relatively slow life history compared to nonprimate mammal taxa. The milk energy from protein of both baboon and macaque (12.8% ± 0.3%) milk was intermediate between the protein milk energy of platyrrhine (19.3%–23.2%) and hominoid (8.9%–12.6%) primates, consistent with their relative growth rates also being intermediate. Compared to these cercopithecid monkeys, platyrrhine primates have both higher relative growth rates and higher milk energy from protein, while apes tend to be lower in both.

1 ∣. INTRODUCTION

The olive baboon (Papio anubis), a species of anthropoid primate within the family Cercopithecidae, is a large semiterrestrial monkey found across most of sub-Saharan Africa (Phillips-Conroy & Jolly, 1986). They are the most widespread of all baboon species (Kunz & Linsenmair, 2008). Their flexible omnivorous diet and diverse foraging strategies aid in their success adapting to the large variety of environments across such a broad distribution (Okecha & Newton-Fisher, 2006). However, like all mammals, infant baboons begin as obligate lactivores and rely upon their mothers' milk to obtain the necessary materials for proper growth and development.

The survival and relative success of the infant is dependent on the availability of milk and proper nutrient allocation, making the composition of breast milk subject to evolutionary pressures to enhance both offspring and maternal fitness (Skibiel et al., 2013). The major constituents of milk include water, protein, fat, sugar, vitamins, and minerals, such as calcium and phosphorus (Jenness, 1988). While these elements are common to all mammal milk, there is significant variation in the relative nutrient proportions across different species and individual mothers within a species (Iverson, 2007; Jenness, 1986; Oftedal, 1984; Oftedal & Iverson, 1995; Skibiel et al., 2013).

A large comparative analysis of milk from 130 species conducted by Skibiel et al. (2013) found that interspecific variation in milk composition was largely described by phylogeny, followed by diet and length of the lactation period. For example, the milk of aardvarks, anteaters, and elephant shrews, three insectivorous species, are similarly high-protein milks, which is consistent with the high-protein maternal diet (Wenker et al., 2019).

Typically, anthropoid primates produce dilute milk with approximately 10%–14% dry matter consisting of around 7% sugar, 1%–4% fat, and 1%–4% protein (Iverson, 2007). Primates generally have a relatively long lactation period with frequent on-demand nursing. Despite this generalization, differences among body size, ecology, and growth and development patterns offer a possible explanation for interspecies variation in milk composition among primates. For example, in marmosets and tamarins, the small body size paired with a rapid reproductive rate and fast infant growth rate is consistent with a higher concentration of milk protein compared to macaques, a larger primate (Milligan, 2010; Power et al., 2002).

There have been few studies on baboon milk composition. The macronutrient composition of baboon milk has yet to be confirmed using modern methods of nutritional analysis and to our knowledge there is no report of specific mineral concentrations. Fat, protein, sugar, dry matter, and ash were previously published in 1968; however, this was not specific to the olive baboon and instead, averaged across multiple baboon species (Buss, 1968).

This study aims to further explore the phylogenetic influence on interspecies milk composition in primates by evaluating the nutritional composition of baboon milk in comparison to milk from another Cercopithecidae species, the rhesus macaque (Macaca mulatta). We predict the milk composition between these two species will show strong similarity. The goals of this study are to (1) characterize the nutritional composition of olive baboon milk, (2) compare baboon milk composition to that of rhesus macaques living at the same institution under identical management conditions, and (3) evaluate the association between milk protein and growth rate within anthropoid primates to explore the relative influence of phylogeny and life history on lactation and milk composition.

2 ∣. METHODS

2.1 ∣. Milk collection

Milk samples were collected from eight female olive baboons and six female rhesus macaques located at the Texas Biomedical Research Institute in San Antonio, TX. Baboons and macaques were group housed, separated by species, and managed under identical conditions. The baboons and macaques were housed in large outdoor cages of various sizes ranging from 300 to 1000 sq. ft. Animals were placed in compatible social groups of approximately 5–20 animals for baboons or approximately 12 individuals for macaques. Animals were provided physical, nutritional, sensory, occupational, and social enrichment. As nutritional enrichment, animals were offered a variety of grains, fruits, vegetables, and other novel food items a minimum of 5 days per week in addition to their regular “monkey chow” diet. The research was approved by IACUC number 1737 MM/PC and complied with US laws and regulations regarding animal research.

Milk sample collection was opportunistic. One milk sample was obtained from each dam during a routine physical examination scheduled on September 15, September 16, or September 22, 2020 for baboons and scheduled on September 1 or September 2, 2020 for macaques. Maternal characteristics, such as age and parity, and day of lactation were recorded and infant age ranged between 47 and 129 days for infant baboons and between 15 and 92 for infant macaques (Table 1). Lactating mothers were removed from the group for examination and sedated with ketamine (10 mg/kg) IM. Mothers were dosed with oxytocin based on weight at 2 IU/kg except for animals weighing more than 10 kg for macaques (1 ml 20 IU top end) and 20 kg for baboons (2 ml 40 IU top end). Milk was manually expressed from both breasts. Milk collection was stopped when streams of milk could no longer be expressed and only drops of milk were present. The collected samples were frozen at −80°C until being shipped on dry ice to the Smithsonian National Zoological Park (SNZP) Nutrition Laboratory in Washington, DC for milk composition analysis. Table 1 lists maternal and infant characteristics as well as total milk volume collected for each animal used in this study.

TABLE 1.

Metadata for the 14 milk samples assayed for this study. Averages are presented as ± SEM

Dam ID	Dam age (years)	Dam weight (kg)	Infant sex	Infant age (days)	Volume collected (ml)
31903	8.2	17.4	F	47	7.4
32132	7.9	20.15	M	59	13.7
28328	14	21.9	M	78	9.5
31299	9.3	24.9	F	93	3.5
28102	14.3	18.4	F	98	6.0
32043	8	22.5	M	107	5.8
33164	6.5	17.6	M	124	5.8
27234	14.9	18.4	M	129	8.9
Baboon average	10.4 ± 1.2	20.2 ± 1.0	–	91.9 ± 10.3	7.5 ± 1.1
32473	7.5	5.67	M	15	1.75
33202	6.4	7.48	M	26	3.0
34270	13.1	9.99	M	41	8.4
34001	6.9	9.91	M	58	2.0
33996	7	10.46	M	87	10.75
33983	7.2	6.64	M	92	3.5
Macaque average	8.0 ± 1.0	8.4 ± 0.8	–	53.2 ± 12.9	4.9 ± 1.5

2.2 ∣. Nutrient assays

All nutrient assays were conducted at the SNZP Nutrition Lab using the standard methods previously developed on location (Hood et al., 2009). Samples were assayed for water (dry matter), fat, total sugar, crude protein (CP), total mineral content (ash), calcium, and phosphorus and all were performed in duplicate or in triplicate. Samples were homogenized by vortex before they were subsampled for procedures. Dry matter, and therefore water content, was determined gravimetrically by weighing samples to 0.001 mg before and after a 3.5 h drying period at 100°C in a forced air drying oven (AOAC, 1990). Dried samples were combusted in a carbon, hydrogen, and nitrogen elemental gas analyzer (Model 2400, Perkin Elmer) to determine total nitrogen (TN) content. TN was used to estimate CP in each milk sample using a conversion factor (TN × 6.38) (Jones, 1931). Total fat was assayed using a micromodification of the Rose-Gottlieb procedure that involves sequential lipid extraction with ethanol, diethyl ether, and petroleum ether (Hood et al., 2009). Total sugar was measured using the phenol-sulfuric acid colorimetric procedure with lactose monohydrate standards and was read at 490 nm on a microplate reader (Model ELX808, Biotek) (Dubois et al., 1956; Marier & Boulet, 1959).

Ash was determined by placing dried milk samples in a muffle furnace at 550°C for 8 h. Individual mineral content for calcium and phosphorus was determined by digesting 700 μl of each milk sample in 20 ml nitric acid and 5 ml of perchloric acid. The resulting digests were diluted with ultrapure distilled deionized water. Calcium was measured using atomic absorption spectroscopy (Model 800 Perkin Elmer Analyst Flame-Furnace Atomic Absorption Spectrophotometer, Perkin Elmer) at 422.7 nm using a nitrous oxide flame (AOAC, 1990). Phosphorus was determined using the AOAC-Modified Gomorri colorimetric method and was read at 450 nm on the same microplate reader used for the sugar assay (AOAC, 1990; Gomorri, 1942).

Milk gross energy (GE) was calculated for each milk sample as the sum of the energy from protein, fat, and sugar using the following energy values: 5.86 kcal/g for protein, 9.11 kcal/g for fat, and 3.95 kcal/g for sugar (Perrin, 1958). This method of GE calculation may be a slight overestimate because it does not account for nonprotein nitrogen. However, this calculated GE value has been shown to closely correlate with experimentally measured gross energy using adiabatic bomb calorimetry for milk from species as diverse as aardvarks (Orycteropus afer, Wenker et al., 2019), bongos (Tragelaphus eurycerus, Petzinger et al., 2014), and rhesus macaques (Macaca mulatta, Hinde et al., 2009).

The calculated GE of each sample was used to calculate the percentage of GE from sugar, fat, and protein for all samples. Thus, we report the macronutrient content of the milk both as percent of the milk (g/100g) and as the percent of GE each macronutrient contributes. For protein we also calculated the mg of protein per kcal of milk.

2.3 ∣. Statistical analysis

All statistical analysis was performed using IBM SPSS software. Milk nutrient values (fat, CP, sugar, DM, ash, Ca, P) are expressed in percentages and averages for a species are expressed as the mean ± SEM in percentage. Pearson's correlation coefficients were used to examine the relationships between individual constituents in baboon milk as well as between the constituents and other characteristics including infant age, infant sex, maternal weight, maternal age, and milk volume collected (significance parameter p < 0.05). Milk composition of baboons was compared to that of rhesus macaques with ANCOVA (significance parameter p < 0.05). Previously published data for milk protein and energy from protein for other primate taxa (Alouatta, Saimiri, Callithrix, Cebuella, Leontopithecus, Cebus, Macaca, Gorilla, Pan, Pongo, Homo) were included to analyze the relationship between the proportion of milk energy from protein and relative growth rate between platyrrhine (fastest growth), cercopithecid (intermediate growth), and hominoid (slowest growth) primates. Published data for each species was used to calculate the average proportion of milk energy from protein for each clade (platyrrhine, cercopithecids, and hominoid) and Bonferroni correction was used to determine significant differences between these groups.

3 ∣. RESULTS

For baboon milk, the average concentrations for fat, protein, and sugar in samples from different females ranging between 47 and 129 days postparturition were 4.7% ± 0.5%, 1.6% ± 0.04%, and 7.3% ± 0.07%, respectively. The total dry matter and ash composition were 14.0% ± 0.6% and 0.16% ± 0.007%. Calcium and phosphorus comprised 49.7% of total mineral content. The concentrations for calcium and phosphorus were 0.048% ± 0.001% and 0.033% ± 0.002% with an average Ca:P ratio of 1.5:1 (Table 2). There were no significant relationships between infant age and constituent composition (Figure 1). Similarly, there were no significant relationships between individual constituents except for phosphorus and fat (p = 0.044) as well as fat and dry matter (p = 0.001).

TABLE 2.

Summary data for macronutrient composition of all samples of baboon milk and macaque milk.

Animal ID	Infant age (Days)	Fat (%)	CP (%)	Sugar (%)	DM (%)	Ash (%)	Ca (%)	P (%)	Ca:P	Gross energy (kcal/g)	% GE from CP (%)
31903	47	2.5	1.5	7.5	11.1	0.16	0.046	0.032	1.4	0.61	14.3
32132	59	3.8	1.8	7.2	13.2	0.18	0.055	0.029	1.9	0.73	14.2
28328	78	5.4	1.5	7.5	15.6	0.15	0.053	0.033	1.6	0.87	10.1
31299	93	5.8	1.6	7.1	14.3	0.13	0.048	0.042	1.2	0.91	10.6
28102	98	4.3	1.6	7.0	13.6	0.18	0.046	0.030	1.5	0.77	12.4
32043	107	7.2	1.5	7.5	16.5	0.15	0.042	0.040	1.1	1.04	8.6
33164	124	4.8	1.8	7.2	14.7	0.19	0.053	0.035	1.5	0.82	12.6
27234	129	4.0	1.5	7.1	13.0	0.18	0.044	0.026	1.7	0.74	11.8
All baboon samples		4.7 ± 0.5	1.6 ± 0.04	7.3 ± 0.07	14.0 ± 0.6	0.16 ± 0.007	0.048 ± 0.001	0.033 ± 0.002	1.5 ± 0.09	0.81 ± 0.04	11.8 ± 0.7
32473	15	3.1	1.6	7.9	13.1	–	–	–	–	0.68	13.6
33202	26	3.3	1.6	7.9	13.2	0.21	0.057	0.033	1.7	0.71	13.2
34270	41	4.9	1.9	7.3	14.5	0.21	0.058	0.032	1.8	0.85	12.9
34001	58	3.2	1.6	7.8	13.2	–	–	–	–	0.69	13.4
33996	87	5.3	1.9	7.6	15.0	0.19	0.052	0.030	1.8	0.89	12.3
33983	92	4.8	1.7	7.7	14.4	0.16	0.050	0.027	1.8	0.84	11.6
All macaque samples		4.1 ± 0.4	1.7 ± 0.05	7.7 ± 0.08	13.9 ± 0.3	0.19 ± 0.01	0.054 ± 0.002	0.031 ± 0.001	1.8 ± 0.02	0.78 ± 0.03	12.8 ± 0.3

FIGURE 1.

Baboon milk constituents showed no significant change across infant age

The mean gross energy of baboon milk was 0.81 ± 0.04 kcal/g. On average, 52% ± 2.6% of the energy contribution was from fat, 12% ± 0.7% from protein, and 36% ± 2.0% from sugar. Energy from fat was positively correlated with the total gross energy of the milk (R = 0.97; p < 0.001) while energy from sugar (R = −0.94; p < 0.001) and energy from protein (R = −0.91; p = 0.002) both were negatively correlated with gross energy (Figure 2). Neither overall gross energy nor the individual energy contributions from each macronutrient showed any significant change across infant age (Figure 3). There were no significant relationships between any constituent of baboon milk and maternal age, infant sex, or milk volume. Gross energy did increase with increasing maternal weight (R = 0.737; p = 0.037) but no other constituent showed a significant relationship with maternal weight.

FIGURE 2.

In baboon milk, the percent of milk GE from fat was positively correlated with the total GE of the milk (R = 0.97; p < 0.001) while energy from sugar (R = −0.94; p < 0.001) and energy from protein (R = −0.91; p = 0.002) both showed a negative correlation with total GE. GE, gross energy

FIGURE 3.

The percent of milk gross energy from protein, sugar, and fat showed no significant change across infant age for both baboon and macaque milk

For macaques, the average concentrations for fat, protein, and sugar in samples from different females ranging between 15 and 92 days postparturition were 4.1% ± 0.4%, 1.69% ± 0.05%, and 7.71% ± 0.08%, respectively. The total dry matter and ash composition were 13.9% ± 0.3% and 0.19% ± 0.01%. Calcium and phosphorus comprised 44.7% of total mineral content. The concentrations for calcium and phosphorus were 0.054% ± 0.002% and 0.031% ± 0.001% with an average Ca:P ratio of 1.8:1 (Table 1). The mean gross energy was 0.78 ± 0.03 kcal/g. On average, 47% ± 2.3% of the energy contribution was from fat, 13% ± 0.3% from protein, and 40% ± 2.0% from sugar. When comparing baboon and macaque milk composition, there was no significant difference between the species average for any constituent on a g for g basis (fat, protein, DM, ash, Ca, P, GE) with the exception of sugar (p = 0.020, df = 1; F = 7.177). When expressed as a percentage of energy (%GE from CP, %GE from sugar, %GE from fat), there was no difference between the two species (Table 3).

TABLE 3.

The only macronutrient that differed significantly between baboon and macaque milk was sugar concentration.

Constituent	Baboon (n = 8)	Macaque (n = 6)	p Value	F-stat (df = 1)
Fat (%)	4.72 ± 0.5	4.10 ± 0.4	ns	0.123
Protein (%)	1.60 ± 0.04	1.69 ± 0.05	ns	2.132
Sugar (%)	7.27 ± 0.07	7.71 ± 0.08	p = 0.02	7.177
DM (%)	14.0 ± 0.6	13.9 ± 0.3	ns	0.927
Ash (%)	0.165 ± 0.007	0.192 ± 0.01	ns	2.510
Ca (%)	0.048 ± 0.001	0.054 ± 0.002	ns	1.624
P (%)	0.033 ± 0.002	0.031 ± 0.001	ns	0.992
GE kcal/g	0.811 ± 0.04	0.777 ± 0.03	ns	0.432
GE from Protein (%)	11.8 ± 0.7	12.8 ± 0.3	ns	0.001
GE from Sugar (%)	36.2 ± 2.0	39.7 ± 2.0	ns	0.115
GE from Fat (%)	51.9 ± 2.6	47.5 ± 2.3	ns	0.082

Abbreviation: GE, gross energy.

The average volume of milk collected from baboons and macaques (Table 1) was not statistically different (df = 1; p = 0.292; F = 1.224). For macaques, the milk volume collected was significantly positively correlated with both protein (R = 0.980, p = 0.001) and fat content (R = 0.851, p = 0.032). Although not significant, there was a tendency for a negative correlation between milk volume and sugar content in macaques (p = 0.103; R = −0.725). There were no significant correlations between volume collected and milk nutrients for baboons.

The proportion of milk energy from protein from the two study species and other platyrrhine and hominid species are presented in Table 4. Milk protein content on an energy basis differed by clade (F = 20.0, df = 11, p < 0.001). Platyrrhine primates had the highest energy from protein (19.9% ± 1.2%) and the hominids the lowest (10.3% ± 0.9%). On an energy basis, platyrrhine milk on average provides 34.6 ± 2.2 mg of protein for every kcal of milk, baboon and macaque milk provides 20.9 ± 0.7 mg/kcal, and hominid milk provides 17.5 ± 1.4 mg/kcal. After Bonferroni correction for multiple comparisons, platyrrhine milk energy from protein was significantly greater than baboon/macaque milk (p = 0.013) and hominid milk (p < 0.001), however hominid and baboon/macaque milk did not differ.

TABLE 4.

Milk protein content (mg/kcal) is positively associated with relative growth rate of simian primates within their taxonomical group, where platyrrhines are the fastest growing, followed by cercopithecids, and then hominids.

Genus	% Protein	% Energy from protein	Milk protein (mg/kcal)	Reference
Alouatta	2.25	23.0	40.2	(Milligan, 2007)
Saimiri	3.59	23.2	39.5	(Milligan et al., 2008)
Callithrix	2.7	20.8	35.5	(Power et al., 2008)
Cebuella	2.9	19.3	36.3	(Power et al., 2002)
Leontopithecus	2.6	17.3	28.9	(Power et al., 2002)
Cebus	2.40	16.0	27.0	(Milligan, 2010)
Macaca	1.95	12.6	21.4	(Hinde et al., 2009)
Macaca	1.69	12.8	21.9	This study
Papio	1.60	11.8	20.2	This study
Gorilla	1.2	12.6	21.3	(Power et al., 2017)
Pan	0.92	10.6	18.1	(Milligan, 2007)
Pongo	0.78	8.9	15.2	(Power et al., 2017)
Homo	1.04	8.9	15.3	(Quinn et al., 2012)

4 ∣. DISCUSSION

This study presents data on the milk macronutrient composition of olive baboons living under human management. Our results are similar to the previous description of baboon milk reported by Buss (1968). Olive baboon milk can be described as a high sugar, low protein, and moderate fat milk, consistent with the dilute milk pattern seen in most primate species and all anthropoid primates (Ben Shaul, 1962; Iverson, 2007). Milk fat demonstrated the highest variation across individuals and protein had the least.

Gross energy of baboon milk was independent of infant age (Figure 3). The contributions to milk energy from fat and sugar were both greater and more variable than the contribution from protein, which was relatively stable. Higher energy milk had a larger percentage of energy coming from fat and a smaller percentage of energy coming from sugar (Figure 2). Protein was consistently the smallest contributor to gross energy and the percent energy from protein was less variable, although it did slightly decrease with increasing gross energy (Figure 2). The low protein on an energy basis is consistent with the relatively slow growth rate of baboons compared to many nonprimate mammal taxa.

The high water, moderate energy content of olive baboon milk is consistent with the species' nursing behavior that involves frequent, on-demand nursing throughout an extended infancy period. This lactation strategy is also common among other nonprimate mammal species that produce dilute milk with low energy and high sugar (Ben Shaul, 1962). On the other hand, mammals that nurse intermittently are known to have milks higher in fat and energy (Hinde & Milligan, 2011; Iverson, 2007; Tilden & Oftedal, 1997). Baboon infants have regular access to the nipple for frequent suckling because their mothers carry them throughout the day. Frequent suckling behavior stimulates lactose production, resulting in increased milk production and reduced milk energy density (Hinde & Milligan, 2011). For mammals living in arid environments, such as baboons on the African savannah, milk is necessary not just for energy but also for maintaining infant hydration. Lactose, the primary sugar in primate milk, osmotically draws water into the mammary gland diluting the milk making it less energetically dense but providing important hydration to the infant.

For primate infants, protein intake is essential for the deposition of lean tissue (e.g., muscle, organ tissue) but also for delivering minerals such as phosphorus and calcium, which are vital for bone growth. Calcium, phosphorus, and protein content in milk are often positively correlated since these two minerals are sequestered in casein protein micelles to deliver high concentrations to the infant without causing mammary gland calcification or mineral precipitation (Holt & Carver, 2012). There were no strong correlations between these constituents in baboon milk noted in this study but that may have been due to the low variation of the minerals and protein as well as the small sample size (Table 2). Despite low concentrations, there was an adequate ratio between the two minerals. To facilitate optimal bone development, it is critical to maintain a proper Ca:P from nutritional intake of 1–2:1 as a low ratio with high phosphorus content would affect calcium bioavailability (Loughrill et al., 2017). The baboons in this investigation had Ca:P ratios that fell within this range, with an average Ca:P of 1.5:1 (Table 1).

The macronutrient composition of baboon and rhesus macaque milk, two Cercopithecidae monkey species, showed strong similarity. These two monkey species are very closely phylogenetically related and diverged into their respective Papio and Macaca lineages during the Late Miocene (Liedigk et al., 2014) approximately 5.3–11.6 mya (Böhme et al., 2008). The only constituent that showed significant difference was the average sugar concentration of milk, which was 7.3% in baboons and 7.7% in macaques (Table 3). However, on an energy basis, the percent of gross energy provided by sugar was not statistically different and no other constituents showed a significant difference between baboon and macaque milk whether expressed as a percent of milk or of milk energy. Our results presented in this study are similar to previously published studies of rhesus macaque milk with much larger sample sizes (Hinde, 2007; Hinde et al., 2009, 2013). Notably, the proportion of energy from protein in macaque milk is virtually identical (Table 3). As an energy source, both macaque and baboon milk are providing the same energy from protein, fat, and sugar content. This similarity in composition is reflective of their closely related phylogeny and other factors such as their similar life history or lactation strategy. We predict that milks of other macaque or baboon species living under human management will be similar to our results for these two species.

We examined if the total milk volume collected affected our results. Although not statistically different, the average volume of milk collected from macaques was smaller than that collected from baboons (Table 1). With smaller volumes, it is possible that the milk collected is not representative of what the infant receives while nursing. For baboons, there were no significant relationships between volume collected and any of the milk constituents. When a larger volume of milk was collected from macaques, there was a significantly higher fat and protein content and a somewhat smaller sugar content.

Across primate species, variation in growth rates generally corresponds with the amount of energy from protein, a pattern evidenced in Table 4. Platyrrhine monkey species typically have rapid growth rates compared to other monkeys and apes (Kirkwood, 1985) and correspondingly have the highest milk protein content (Milligan, 2007, 2010; Milligan et al., 2008; Power et al., 2002, 2008). Within this group, Cebus monkeys have uniquely slow postnatal growth rates compared to other platyrrhine monkeys (Marriog, 2007). Consistent with this, Cebus monkeys also have a lower protein contribution to milk energy compared to other platyrrhine species here (Table 4).

Orangutans, on the other hand, are known to have the longest life history of nonhuman primates and very slow growth rates (Wich et al., 2004). Their milk composition reflects this with a comparatively low milk protein content whether expressed as percent of milk or of milk energy (Power et al., 2017). Gorilla milk has a low protein concentration compared to cercopithecids, which is expected for a great ape. However, because the milk is so dilute, the relative energy from protein and the milk protein on a mg/kcal basis falls in the range of Cercopithecidae monkeys (Table 4). Gorillas are the fastest growing apes in the Hominidae family (Leigh & Shea, 1996), which is consistent with having the highest milk protein energy among hominids.

Baboons and macaques both fall roughly between hominids and platyrrhines in both growth rates and milk energy from protein. As a group, Cercopithecidae monkey species have similar life histories in that they mature relatively late and develop a larger body size compared to other monkey species and the majority of brain growth happens during the prenatal period (whereas in hominids and plathyrrines, a large amount of brain growth occurs during the postnatal period) (Leigh, 2004). After accounting for size, platyrrhines have the fastest growth rates, followed by Cercopithecidae, and then great apes (Kirkwood, 1985). The baboon and macaque data presented in this paper fit within this suggested pattern of energy from protein corresponding with the relative growth rates of primates.

It is important to note that the results presented in this investigation may not be indicative of wild olive baboon populations since the samples were obtained from captive baboons. Animals living in captivity often have regular access to food and consume a diet different from their wild conspecifics, which could affect body condition. In common marmosets, maternal body condition affected fat concentration of milk as well as infant growth rate (Tardif et al., 2001). However, Roberts et al. (1985) showed no changes in baboon milk composition when the mothers were placed on restricted diets.

A limitation of this study was the small sample size and the fact that each sample was taken from a different lactating baboon. Having samples from unique mothers is valuable because it includes a broader range of animals whose individual characteristics might cause slight changes in milk; however, it presents challenges in drawing conclusions about changes across lactation. Especially with a small sample size, it can be unclear if the variation in composition is due to the infant age or simply individual variations between baboon mothers. However, this study strongly benefits from including baboon and macaque mothers living at the same institution and under the same management conditions, making comparisons between the milks of each species more reliable. Future studies investigating the composition of baboon milk should include longitudinal samples taken at several points over the course of lactation from the same female to make more accurate conclusions about changes over lactation.

5 ∣. CONCLUSIONS

• The high water, moderate energy milk is consistent with baboon lactation strategy.

• Baboon milk composition shows strong similarity to that of rhesus macaque milk, implying that other baboon and macaque species living under human management will produce similar milk.

• The energy from protein is consistent with the growth rate of baboons and other Cercopithecidae being intermediate between that of platyrrhines and hominids.

DATA AVAILABILITY STATEMENT

Data are available from the authors upon reasonable request.