Excretion patterns of solute and different-sized particle passage markers in foregut-fermenting proboscis monkey (Nasalis larvatus) do not indicate an adaptation for rumination

Matsuda, Ikki; Sha, John Chih Mun; Ortmann, Sylvia; Schwarm, Angela; Grandl, Florian; Caton, Judith; Jens, Warner; Kreuzer, Michael; Marlena, Diana; Hagen, Katharina B; Clauss, Marcus

doi:10.1016/j.physbeh.2015.05.020

Cited by 83 publications

(28 citation statements)

References 44 publications

(86 reference statements)

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“…The results for ponies are in line with those for other large, nonruminant foregut fermenters including macropods, peccaries, hippos and colobine monkeys, in which no selective retention of a certain particle size fraction was observed (Matsuda et al, 2015;Munn, Tomlinson, Savage, & Clauss, 2012;Schwarm, Ortmann, Wolf, Streich, & Clauss, 2009;Schwarm et al, 2008). Anyhow, a selective retention of large particles in a non-ruminant herbivore appears unlikely.…”

Section: Discussionsupporting

confidence: 83%

Comparative selective retention of particle size classes in the gastrointestinal tract of ponies and goats

Hummel

Scheurich

Ortmann

et al. 2017

Animal Physiology Nutrition

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There is a discrepancy in the literature on potential digesta separation mechanisms in horses, with both a selective retention of fine and of large particles postulated in different publications. To assess the net effect of such mechanisms, we fed ponies on a hay-only diet a pulse dose of whole (unchopped) marked hay together with a solute marker, collected faeces on a regular basis, measured marker concentrations in whole faeces and in their large (2.0-16 mm), medium (0.5-1.0 mm) and small (0.063-0.25 mm) particle fraction, and calculated the corresponding mean retention times (MRTs). For comparison, the same experiment was performed in goats. In goats, as expected, MRT (35 hr) was significantly shorter than MRT (51 hr); only a very small fraction of particle marker was excreted as large particles (2%); and the MRT of these large particles was significantly shorter than that of small particles (with a relevant difference of 8.6 hr), indicating that those few large particles that escape the rumen do so mostly soon after ingestion. In ponies, MRT (24 hr) did not differ from MRT (24 hr); a higher fraction of particle marker was excreted as large particles (5%); and the MRT of these large particles was longer than that of small particles (but with a non-relevant difference of less than 1 hr). These results indicate that no relevant net separation of digesta phases occurs in horses and that selective particle retention mechanisms in the large intestine are unlikely to represent important characteristics of the horse's digestive physiology.

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Section: Discussionsupporting

confidence: 83%

Comparative selective retention of particle size classes in the gastrointestinal tract of ponies and goats

Hummel

Scheurich

Ortmann

et al. 2017

Animal Physiology Nutrition

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“…Foregut‐fermenters are known to exhibit mechanisms for optimizing nutrient intake through, for example, particle size reduction, digesta retention, and food intake (Fritz et al, ; Müller et al, ). While we do not have information on particle passage through the gut of red‐shanked doucs, it was shown in proboscis monkeys that the sequestration of digesta can occur either in the forestomach or in the cecum and colon, thus the gut is not adapted to a selective retention of particles of a specific size (Matsuda et al, ). Owing to the red‐shanked doucs' captive diet, it could also be expected for foregut particle sizes to be smaller than their wild conspecifics, thus reducing the function of the foregut for processing such easily digestible food materials and as a consequence, lowering bacterial diversity.…”

Section: Discussionmentioning

confidence: 94%

Bacterial community structure and function distinguish gut sites in captive red‐shanked doucs (Pygathrix nemaeus)

Clayton

Shields-Cutler

Hoops

et al. 2019

American J Primatol

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The mammalian order primates contains wide species diversity. Members of the subfamily Colobinae are unique amongst extant primates in that their gastrointestinal systems more closely resemble those of ruminants than other members of the primate order. In the growing literature surrounding nonhuman primate microbiomes, analysis of microbial communities has been limited to the hindgut, since few studies have captured data on other gut sites, including the foregut of colobine primates. In this study, we used the red-shanked douc (Pygathrix nemaeus) as a model for colobine primates to study the relationship between gastrointestinal bacterial community structure and gut site within and between subjects. We analyzed fecal and pregastric stomach content samples, representative of the hindgut and foregut respectively, using 16S recombinant DNA (rDNA) sequencing and identified microbiota using closed-reference operational taxonomic unit (OTU) picking against the GreenGenes database. Our results show divergent bacterial communities clearly distinguish the foregut and hindgut microbiomes. We found higher bacterial biodiversity and a higher Firmicutes:Bacteroides ratio in the hindgut as opposed to the foregut. These gut sites showed strong associations with bacterial function. Specifically, energy metabolism was upregulated in the hindgut, whereas detoxification was increased in the foregut.Our results suggest a red-shanked douc's foregut microbiome is no more concordant with its own hindgut than it is with any other red-shanked douc's hindgut microbiome, thus reinforcing the notion that the bacterial communities of the foregut and hindgut are distinctly unique. K E Y W O R D S colobine, ecology, microbiome, primate 1 | INTRODUCTION Understanding the structure and function of the gut microbiome in our closest evolutionary relatives, nonhuman primates, has the potential to shed light on how we have coevolved with our own gut microbiomes. While humans and nonhuman primates are closely related, there are major species-to-species differences in appearance and behavior, including countless differences in dietary preference.Of specific interest are the colobines, which have unique anatomy, physiology, and ecology, compared with noncolobine extant primates.Colobines are folivorous Old World monkeys with specialized gastrointestinal (GI) systems that bear close resemblance to those of ruminants, allowing them to exploit feeding niches unique among primates

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“…However, experiments with captive colobines with different-sized digesta markers suggest there is no particle-sorting mechanism (Schwarm et al 2009). Even in the proboscis monkey (Nasalis larvatus)t h a tr u m inates (Matsuda et al 2011), which should result in particularly efficient digesta particle size reduction (Matsuda et al 2014b), no sorting mechanism is evident when they are fed passage markers of different sizes (Matsuda et al 2015). However, if other factors related to the presence of a forestomach constrain resting position, then we would expect a similar predominance of a sitting resting position in colobines.…”

Section: Introductionmentioning

confidence: 99%

Primate Resting Postures: Constraints by Foregut Fermentation?

Matsuda

Chapman

Chua

et al. 2017

Physiological and Biochemical Zoology

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Although resting is one of the dominant behaviors of foregut-fermenting primates (i.e., colobines), their resting posture has rarely received attention. We hypothesize that colobines are more constrained in their resting position than hindgut-fermenting primates and that colobines assume a sitting resting position for specific reasons. To test this hypothesis, we followed two approaches. First, we observed resting positions in two captive individuals each of eight species and tested whether colobines rested in a sitting position more than other primates. Second, we collected literature data on free-ranging specimens of 31 species and again tested whether colobines rested in a sitting position more than other primates. Both approaches indicated that colobines spent more time in a sitting posture than other primates (73.0% vs. 23.2% in captivity and 83.0% vs. 60.9% in the wild, respectively). We hypothesize that the position of the digestive chamber and the necessity of frequently having to eructate digestion gases force colobines to take a sitting posture to avoid pressure on the thorax and respiratory organs.

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Excretion patterns of solute and different-sized particle passage markers in foregut-fermenting proboscis monkey (Nasalis larvatus) do not indicate an adaptation for rumination

Cited by 83 publications

References 44 publications

Comparative selective retention of particle size classes in the gastrointestinal tract of ponies and goats

Comparative selective retention of particle size classes in the gastrointestinal tract of ponies and goats

Bacterial community structure and function distinguish gut sites in captive red‐shanked doucs (Pygathrix nemaeus)

Primate Resting Postures: Constraints by Foregut Fermentation?

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