In Vitro Fermentation of Dietary Carbohydrates Consumed by African Apes and Monkeys: Preliminary Results for Interpreting Microbial and Digestive Strategy

Abstract

Primates derive significant nutritional benefits from hosting symbiotic, fermenting microbes in their gut, including the provision of energy from short-chain fatty acids (SCFAs). We measured fermentation parameters in fecal samples of 4 hindgut fermenting species (Gorilla gorilla, Pan troglodytes, Papio hamadryas, Cercopithecus neglectus) and 1 foregut fermenting species (Colobus guereza) to determine whether differences in SCFA profiles exist between the 2 digestive systems. We analyzed SCFA profiles, culture pH, and methane from fecal samples collected at the North Carolina Zoological Park. Results indicate that the captive individuals exhibit high total SCFA concentrations, with a particularly high acetateto-propionate ratio. Methane levels were highest in the 2 ape species, and lowest in Colobus guereza and Cercopithecus neglectus. Total SCFA concentrations were similar between wild and captive-born Gorilla gorilla, although concentrations of acetate were significantly greater -and butyrate concentration and methane production significantly lower-in wild-caught gorillas relative to captive-born. These results are consistent with data on diet and digestive retention times among Catarrhini and have implications for our understanding of the interactions among diet, body mass, digestion, and how monogastric cercopithecines can consume either similar or greater levels of fiber than larger-bodied apes.

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

“…Howlers can consume a leaf-heavy diet (Milton, 1980;Lambert, 1998;Estrada and Coates-Estrada, 2005;Di Fiore and Campbell, 2007), permitting them to occupy areas with limited resource availability and to persist longer in degraded habitats than more frugivorous primate taxa (Estrada and Coates-Estrada, 1996;Zunino et al, 2007). As many leaves contain high levels of resistant fiber and toxins, GI microbiome contributions to daily energy flows through metabolism of xenobiotics are critical to howler nutrition (Milton, 1979;Lambert, 1998;Lambert and Fellner, 2012). Fibrolytic processes of the GI microbiome contribute up to 31% of a howler's required daily energy via the formation of short-chain fatty acids (93.7% acetate, 5.9% propionate, 0.4% butyrate in A. palliata ;Milton and McBee, 1983).…”

The Howler Monkey as a Model for Exploring Host-Gut Microbiota Interactions in Primates

“…Like all mammals, primates rely on their gut microbiota to process low-quality resources such as woody plants, mature leaves, fungi, and plant exudates that are diffi cult to digest and require greater handling and processing due to mechanical defenses, limited nutrients, and high concentrations of indigestible material or toxins (Lambert 2011 ). As a result, in addition to adaptations in dental morphology, specialized features of either the foregut or the hindgut have evolved independently in species of prosimians (indriids, Lepilemur ), New World monkeys ( Alouatta , Callithrix ), Old World monkeys (colobines), and apes (gorillas) that regularly exploit low-quality resources.…”

Evolutionary Biology of Ape and Monkey Feeding and Nutrition

“…These monkeys generally do not consume arthropods for dietary protein, and while some colobine species consume unripe fruit pulp, an alkaline forestomach pH (and the potential for acidosis) precludes colobines from consuming high levels of ripe fruit (Kay and Davies 1994). However, because of their specialized foregut fermentation strategy (see next section), colobines can very efficiently digest plant foods with high levels of both fiber and secondary metabolites not consumed by sympatric cercopithecines or apes (Kay and Davies 1994;Lambert 1998Lambert , 2002bLambert and Fellner 2012).…”

“…The dietary differences among monkeys and great apes of the Old World can be explained by alternative digestion, fermentation, and detoxification systems in Cercopithecoidea and African apes (Lambert and Fellner 2012).…”

“…Plant cell walls require considerable fermentation before they are useful as an energy source, and longer digestive retention times result in more fermentation (Milton 1981(Milton , 1984(Milton , 1986(Milton , 1993Lambert 1998;Remis 2000;Lambert and Fellner 2012). It is typically argued that "both the total capacity of the digestive tract and the capacity available for microbial fermentation are almost directly proportional to body mass" and that only an increase in body size would allow longer Handbook of Paleoanthropology DOI 10.1007/978-3-642-27800-6_39-3 # Springer-Verlag Berlin Heidelberg 2013 retention times (Cork and Foley 1991, p. 139;Kay and Davies 1994).…”