title: The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra).
abstract: In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male (N = 4), adult female (N = 4), and juvenile (N = 5) wild black howler monkeys (Alouatta pigra) across a ten-month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host-microbe relationships in primate evolution.
authors.affiliation: Program in Ecology, Evolution, and Conservation Biology, University of Illinois, Urbana, IL, 61801; Department of Anthropology, University of Colorado, Boulder, CO, 80309.
authors.forename: Katherine R
authors.initials: KR
authors.lastname: Amato
authors.forename: Steven R
authors.initials: SR
authors.lastname: Leigh
authors.forename: Angela
authors.initials: A
authors.lastname: Kent
authors.forename: Roderick I
authors.initials: RI
authors.lastname: Mackie
authors.forename: Carl J
authors.initials: CJ
authors.lastname: Yeoman
authors.forename: Rebecca M
authors.initials: RM
authors.lastname: Stumpf
authors.forename: Brenda A
authors.initials: BA
authors.lastname: Wilson
authors.forename: Karen E
authors.initials: KE
authors.lastname: Nelson
authors.forename: Bryan A
authors.initials: BA
authors.lastname: White
authors.forename: Paul A
authors.initials: PA
authors.lastname: Garber
mesh_terms: D000204:Activity Cycles; D000508:Alouatta / Q000382:microbiology* / Q000502:physiology*; D000596:Amino Acids / Q000032:analysis; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D002241:Carbohydrates / Q000032:analysis; D004032:Diet; D002149:Energy Intake / Q000502:physiology*; D005227:Fatty Acids / Q000032:analysis; D005243:Feces / Q000737:chemistry / Q000382:microbiology; D005260:Female; D041981:Gastrointestinal Tract / Q000382:microbiology*; D008297:Male; D064307:Microbiota
chemical_list: D000596:Amino Acids; D002241:Carbohydrates; D005227:Fatty Acids
keywords: compensation; growth; gut microbiome; nonhuman primate; reproduction