Faecal particle size in free-ranging primates supports a ‘rumination’ strategy in the proboscis monkey (Nasalis larvatus)

Matsuda, Ikki; Tuuga, Augustine; Hashimoto, Chie; Bernard, Henry; Yamagiwa, Juichi; Fritz, Julia; Tsubokawa, Keiko; Yayota, Masato; Murai, Taichi; Iwata, Yuji; Clauss, Marcus

doi:10.1007/s00442-013-2863-9

Cited by 37 publications

(61 citation statements)

References 59 publications

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“…Moir et al 1954;Bauchop and Martucci 1968), but the process of rumination clearly sets ruminants apart from non-ruminant foregut fermenters (Fritz et al 2009;Schwarm et al 2009b;Clauss et al 2010). True rumination has evolved in only two artiodactyl lineages, the ruminants and the camelids, while sporadic regurgitation and repeated mastication of stomach contents (merycism) have been reported in a variety of mammals such as koala (Phascolarctos cinereus) (Logan 2001(Logan , 2003, macropods (Moir et al 1956;Mollison 1960;Barker et al 1963;Hendrichs 1965), hyrax (Procavia capensis) (Hendrichs 1965), capybara (Hydrochoerus hydrochaeris) (Lord 1994), and proboscis monkeys (Nasalis larvatus) (Matsuda et al 2011(Matsuda et al , 2014. In contrast to merycism, rumination is an obligatory, regular behavioural Abstract The mean retention times (MRT) of solute or particles in the gastrointestinal tract and the forestomach (FS) are crucial determinants of digestive physiology in herbivores.…”

Section: Introductionmentioning

confidence: 99%

Digesta retention patterns of solute and different-sized particles in camelids compared with ruminants and other foregut fermenters

Dittmann

Runge²,

Ortmann

et al. 2015

J Comp Physiol B

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The mean retention time (MRT) of solute or particles in the gastrointestinal tract (GIT) and the forestomach (FS) are crucial determinants of digestive physiology in herbivores. Besides ruminants, camelids are the only herbivores that have evolved rumination as an obligatory physiological process consisting of repeated mastication of large food particles, which requires a particle sorting mechanism in the FS. Differences between camelids and ruminants have hardly been investigated so far. In this study we measured MRTs of solute and differently-sized particles (2, 10, and 20 mm), and the ratio of large-to-small particle MRT, i.e., the selectivity factors (SF10/2mm, SF20/2mm, SF20/10mm), in three camelid species: alpacas (Vicugna pacos), llamas (Llama glama), and Bactrian camels (Camelus bactrianus). The camelid data were compared with literature data from ruminants and non-ruminant foregut fermenters (NRFF). Camelids and ruminants both had higher SF10/2mmFS than NRFF, suggesting convergence in the function of the FS sorting mechanism in contrast to NRFF, in which such a sorting mechanism is absent. The SF20/10mmFS did not differ between ruminants and camelids, indicating that there is a particle size threshold of about 1 cm in both suborders above which particle retention is not increased. Camelids did not differ from ruminants in MRT2mmFS, MRTsoluteFS and the ratio MRT2mmFS/MRTsoluteFS, but they were more similar to 'cattle-' than to 'moose-type' ruminants. Camelids had higher SF10/2mmFS and higher SF20/2mmFS than ruminants, indicating a potentially slower particle sorting in camelids than in ruminants, with larger particles being retained longer in relation to small particles. sorting mechanism in contrast to NRFF, in which such a sorting mechanism is absent. The SF 20/10mm FS did not differ between ruminants and camelids, indicating that there is a particle size threshold of about 1 cm in both suborders above which particle retention is not increased. Camelids did not differ from ruminants in MRT 2mm FS, MRT solute FS, and the ratio MRT 2mm FS/MRT solute FS, but they were more similar to 'cattle-' than to 'moose-type' ruminants. Camelids had higher SF 10/2mm FS and higher SF 20/2mm FS than ruminants, indicating a potentially slower particle sorting in camelids than in ruminants, with larger particles being retained longer in relation to small particles.

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Section: Introductionmentioning

confidence: 99%

Digesta retention patterns of solute and different-sized particles in camelids compared with ruminants and other foregut fermenters

Dittmann

Runge²,

Ortmann

et al. 2015

J Comp Physiol B

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“…This increased chewing efficiency is not achieved by a particular dental design, but by a density-depending sorting mechanism in the forestomach, which separates the small particles from the large ones that are then regurgitated to be masticated again (i.e., rumination) (Lechner-Doll et al, 1991). Although merycism (i.e., regurgitation and re-mastication) and the presence of comparatively fine digesta particles have been reported in non-ruminant foregut fermenters such as kangaroos Vendl et al, 2017) and proboscic monkeys (Nasalis larvatus) (Matsuda et al, 2011;Matsuda et al, 2014), true rumination linked to a sorting mechanism and with a physiologically fixed motor sequence (Gordon, 1968) only evolved twice, in the camelids and the taxonomic ruminants. While there appears to be no functional difference in the forestomach particle sorting mechanism between these two functional ruminant groups (Dittmann et al, 2015b), a major difference between them is the generally lower metabolism and lower feed intake in camelids (Dittmann et al, 2014).…”

Section: Basic Ruminant Digestive Physiologymentioning

confidence: 99%

Physiological adaptations of ruminants and their potential relevance for production systems

Clauss

Hummel

2017

R. Bras. Zootec.

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-Herbivores face the dilemma that the level of feed intake is negatively related to factors that determine digestive efficiency, such as thoroughness of ingesta comminution by chewing, and retention of digesta in the digestive tract. Ruminants have evolved particular adaptations to solve this dilemma. Most ruminants share the characteristic of "digesta washing": fluid moves through their digestive tract faster than particles, thus effectively washing very fine particles, such as bacteria, out of the digesta plug. As the forestomach is followed by auto-enzymatic digestion, this allows a continuous, increased harvest of microbes from the forestomach. True rumination only evolved twice, in the camelids and the true ruminants. These both evolved a density-dependent sorting mechanism based on physical separation of the digesta by the process of flotation and sedimentation, ensuring that the process of rumination is applied to large particles. Differences in this sorting mechanism might facilitate a faster digesta processing in true ruminants as compared with camelids. The hallmark of ruminant digestive anatomy is the omasum, in which the fluid required for both digesta washing and the reticular separation mechanism is re-absorbed. In ruminants of the tribe Bovini, the omasum has reached the largest size and this group has a particularly great forestomach fluid throughput. Increasing the degree of digesta washing even more should increase microbial harvest from the forestomach and reduce the susceptibility to acidosis. At the same time, it should result in a metabolic state of the microbiome more tuned towards biomass production and less towards methanogenesis. Enhancing the forestomach fluid throughput by selective breeding could represent a promising way to further advance the productivity of the ruminant digestive tract.

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“…Measuring faecal particle size by wet sieving analysis is an established non-invasive approach to determine the chewing efficiency of mammals [Fritz et al, 2009]. Several studies have focused on faecal particle size in mammals [Fritz et al, 2009;Clauss et al, 2015], or more specifically in ruminants [Renecker and Hudson, 1990;Clauss et al, 2002] and primates [Dunbar and Bose, 1991;Matsuda et al, 2014;Venkataraman et al, 2014;Weary et al, 2017]. Across mammals, the size of faecal particles usually increases with animal body mass [Fritz et al, 2009].…”

Section: Introductionmentioning

confidence: 99%

Faecal Particle Size in Free-Ranging Proboscis Monkeys, Nasalis larvatus: Variation between Seasons

Thiry¹,

Clauss²,

Stark³

et al. 2018

IJFP

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Reducing the size of food particles is crucial for herbivores. Seasonal dietary changes are known to influence animals’ chewing efficiency. Proboscis monkeys (Nasalis larvatus) are foregut fermenters, with a high chewing efficiency allowing them to achieve very fine faecal particles. In this study, we investigated how proboscis monkeys’ chewing efficiency varies between wet and dry seasons, hypothesising differences possibly related to diet change. Faecal particle size analysis is an established approach to estimate chewing efficiency in mammalian herbivores. We analysed 113 proboscis monkey faecal samples collected in the Lower Kinabatangan Wildlife Sanctuary, between 2015 and 2017. By following standard sieve analysis protocols, we measured a mean particle size MPS_0.025–8 of 0.45 ± 0.14 mm, and confirmed a previous result that proboscis monkeys have a very low faecal MPS. This study highlights a seasonal influence on proboscis monkeys’ chewing efficiency, with smaller MPS (better chewing efficiency) during the wet season. During that time of the year, individuals may potentially change their diet, as all faecal samples contained intact seeds. Whether the seasonal MPS difference in proboscis monkeys is smaller than in other colobines due to their “rumination” strategy remains to be investigated.

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Faecal particle size in free-ranging primates supports a ‘rumination’ strategy in the proboscis monkey (Nasalis larvatus)

Cited by 37 publications

References 59 publications

Digesta retention patterns of solute and different-sized particles in camelids compared with ruminants and other foregut fermenters

Digesta retention patterns of solute and different-sized particles in camelids compared with ruminants and other foregut fermenters

Physiological adaptations of ruminants and their potential relevance for production systems

Faecal Particle Size in Free-Ranging Proboscis Monkeys, Nasalis larvatus: Variation between Seasons

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