Patterns of milk macronutrients and bioactive molecules across lactation in a western lowland gorilla (Gorilla gorilla) and a Sumatran orangutan (Pongo abelii)

Abstract

In addition to nutrients, milk contains signaling molecules that influence offspring development. Human milk is similar in nutrient composition to that of apes, but appears to differ in other aspects such as immune function. We examine the longitudinal patterns across lactation of macronutrients, the metabolic hormone adiponectin, the growth factors epidermal growth factor (EGF) and transforming growth factor β2 (TGF-β2), and two receptors for these growth factors (EGF-R and TGF-β2-RIII) in milk samples collected between days 175 and 313 postpartum from a Sumatran orangutan (Pongo abelii) and between days 3 and 1,276 from a western lowland gorilla (Gorilla gorilla), and compare the results with human data from the literature. Milk macronutrients and hormones were measured using standard nutritional assays and commercially available enzyme immunoassay kits. Ape milk fat content was lower than human milk values, but protein and sugar were similar. Concentrations of all bioactive molecules were consistently detectable except for TGF-β2 in orangutan milk. Concentrations of adiponectin, EGF, and TGF-β2 in both ape milks were lower than found in human breast milk. Concentrations declined with infant age in orangutan milk; in gorilla milk concentrations were high in the first months, and then declined to stable levels until 2-3 years after birth when they increased. However, when expressed on a per energy basis milk constituent values did not differ with age for orangutan and the variation was reduced at all ages in gorilla. In orangutan milk, the ratio of EGF-R to EGF was constant, with EGF-R at 7.7% of EGF; in gorilla milk the EGF-R concentration was 4.4 ± 0.2% of the EGF concentration through 3 years and then increased. These data indicate that potent signaling molecules such as EGF and adiponectin are present in ape milk at physiological concentrations. However, human breast milk on average contains higher concentrations.

Diversity and temporal dynamics of primate milk microbiomes

“…This indicates that the bacterial community was gradually turning over with time. Nutrient content is largely stable in mature milk intra‐individually (Garcia et al, ; Hinde et al, ; Power et al, ), and we found no association of nutrient content predicting changes in the microbiome over time. Instead these changes over time may reflect EMT moving different bacteria from the mother's gut to the mammary gland and/or changes in the infant oral microbiome over time (Dzidic et al, ) that changes which bacteria colonize milk through retrograde flow during suction (Ascinar et al, ; Biagi et al, ).…”

“…Milk samples for nonhuman primates were collected either voluntarily or while under anesthesia. Samples were collected with approved protocols from NZP IACUC and Zoo Atlanta Scientific Review Committee for western lowland gorillas, Bornean orangutans ( Pongo pygmaeus ), and Sumatran orangutans (Garcia, Power, & Moyes, ; Power et al, ) and UCLA and UC Davis IACUCs for rhesus macaques ( Macaca mulatta ; Hinde, Power, & Oftedal, ). Bonobo ( Pan paniscus ), chimpanzee ( Pan troglodytes ), and owl monkey ( Aotus nancymaae ) samples were collected as part of standard management procedures in accordance with institutional guidelines for care and use of animals at their respective facilities (see Table ).…”

“…We leveraged existing metadata of milk nutrient composition, energetic density, and hormone concentration from previous research (Anderson et al, ; Garcia et al, ; Hinde et al, ; Power et al, ; Quinn et al, ). We previously assayed a subset of samples using standard nutrient composition methods to calculate % crude protein, % total sugar, and % crude fat (Garcia et al, ; Hinde et al, ; Power et al, ). For the species comparison data set, we had nutrient assay data available for five species (sample n = 45; Table ).…”

“…For the species comparison data set, we had nutrient assay data available for five species (sample n = 45; Table ). For the data derived from longitudinal milk sampling (Table ), we had nutrient assay results for two mothers, Mandara ( n = 15) and Sarah ( n = 8; Garcia et al, ; Power et al, ) . Gross energy (GE) was calculated for each milk sample using the formula: GE = (9.11 kcal/g * % fat + 5.86 kcal/g * % crude protein + 3.95 kcal/g * % sugar)/100 (Hinde et al, ; Petzinger et al, ; Power, Watts, Murtough, & Knight, ).…”

Immunoglobulin A and nutrients in milk from great apes throughout lactation

“…For the National Zoo gorilla in this study, many samples that were collected were from a complete evacuation of the mammary gland. There was no effect of whether the mammary expression was full or partial for any measured milk nutrient or the hormones adiponectin, epidermal growth factor, and transforming growth factor β‐2 (Power et al, ). The composition of a large milk sample (>30 ml) collected from the Pongo pygmaeus female under anesthesia from a prior birth (Milligan, ) was identical to the composition of the two small samples collected for this study.…”