Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots ( Marmota marmota )

Hume, David; Beiglböck, Christoph; Ruf, T.; Frey-Roos, Fredy; Bruns, Ute; Arnold, Walter

doi:10.1007/s00360-001-0240-1

Cited by 86 publications

(17 citation statements)

References 37 publications

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“…The major difference in the SCFA profile of the cecum and proximal colon of wallabies fed pellets compared with those fed hay was that they had greater proportions of n-butyrate (Table 3). Butyrate is involved in the trophic responses of the gastrointestinal tracts of numerous mammal species, including humans (Sakata 1987(Sakata , 1995Hume et al 2002), and we have now shown that it may also be involved in hindgut plasticity in a marsupial herbivore. How feed particle size is involved with butyrate production is uncertain, but it must involve the intestinal microbiome in some way.…”

Section: Discussionmentioning

confidence: 79%

“…Remarkable plasticity of the gut has been observed in a wide variety of vertebrate species, including carnivores (e.g., Secor and Diamond 1998;Starck and Beese 2001;Starck 2005), omnivores (e.g., Derting 1996;Karasov and McWilliams 2005), and herbivores (e.g., Gross et al 1985;Hammond and Wunder 1991) and under a range of circumstances, including long-distance migrations in birds (e.g., Piersma et al 1999;Karasov et al 2004), diet switching in birds (e.g. , Starck 1999a;van Gils et al 2003) and mammals (e.g., Gross et al 1985;Hammond and Wunder 1991), and after arousal from hibernation (e.g., Hume et al 2002;see also Carey 2005). In mammals at least, the gut is arguably the most energetically expensive organ system to maintain, contributing disproportionately to basal metabolism and whole-body protein turnover (Stevens and Hume 1995).…”

Section: Hindgut Plasticity In Wallabies Fed Hay Either Unchopped or mentioning

confidence: 99%

“…Mammalian herbivores cannot autoenzymatically break down plant fiber; instead, they rely on its fermentation by intestinal microbes to yield short-chain fatty acids (SCFAs) that are absorbed and metabolized by the host (Stevens and Hume 1995). Some SCFAs stimulate gut-cell proliferation (Sakata 1995) and have been correlated with changes in organ mass, particularly of the hindgut (e.g., Hume et al 2002). Consequently, studies of herbivore gut plasticity usually focus on the fiber content of whole diets, but other factors such as plant-cell contents (e.g., proteins, soluble sugars) and/or feed particle size might be involved.…”

Section: Hindgut Plasticity In Wallabies Fed Hay Either Unchopped or mentioning

confidence: 99%

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Hindgut Plasticity in Wallabies Fed Hay either Unchopped or Ground and Pelleted: Fiber Is Not the Only Factor

Munn

Clissold²,

Tarszisz³

et al. 2009

Physiological and Biochemical Zoology

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Phenotypic plasticity of the gastrointestinal tract is crucial for optimal food processing and nutrient balance in many vertebrate species. For mammalian herbivores, gut plasticity is typically correlated with the fiber content of forage; however, we show here that other factors such as ingesta particle size may effect profound phenotypic plasticity of the fermentative hind-gut in a medium-sized (10-kg body mass) marsupial herbivore, the red-necked wallaby (Macropus rufogriseus). When dietary fiber contents were comparable, red-necked wallabies that were fed a finely ground, pelleted hay for 60-72 d had hindguts that were some 28% heavier (empty wet mass) than those fed unchopped hay. The hindguts of pellet-fed wallabies contained more wet ingesta, which was also of a finer particle size, than those fed hay, indicating some separation of large-and small-particle fermentation between the foregut and the hindgut, respectively. Such a digestive strategy would benefit animals by allowing fermentation of a range of ingesta particle sizes that are expected for free-ranging animals faced with a spectrum of diet types and qualities. The heavier hindgut of pellet-fed wallabies was correlated with increased concentrations of short-chain fatty acids (SCFAs) in the fermentative hindgut (cecum and proximal colon) and particularly with increases in the molar proportions of n-butyric acid. The mechanisms facilitating gut plasticity in herbivorous mammals are uncertain, but we suggest that manipulating ingesta particle size rather than dietary fiber could provide a useful tool for evaluating causal explanations. In particular, altering ingesta particle size could help to distinguish possible direct processes (e.g., the favoring of smaller intestinal microbes and production of specific SCFAs) from indirect affects of feed structure (e.g., muscular hypertrophy to compensate for increased intakes and digesta bulk or the fermentation of mucus secreted to promote the flow of viscous, fine-particle material). ABSTRACT Phenotypic plasticity of the gastrointestinal tract is crucial for optimal food processing and nutrient balance in many vertebrate species. For mammalian herbivores, gut plasticity is typically correlated with the fiber content of forage; however, we show here that other factors such as ingesta particle size may effect profound phenotypic plasticity of the fermentative hindgut in a medium-sized (10-kg body mass) marsupial herbivore, the red-necked wallaby (Macropus rufogriseus). When dietary fiber contents were comparable, red-necked wallabies that were fed a finely ground, pelleted hay for 60-72 d had hindguts that were some 28% heavier (empty wet mass) than those fed unchopped hay. The hindguts of pellet-fed wallabies contained more wet ingesta, which was also of a finer particle size, than those fed hay, indicating some separation of large-and smallparticle fermentation between the foregut and the hindgut, respectively. Such a digestive strategy would benefit animals by allowing fermentation of a range of in...

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Section: Discussionmentioning

confidence: 79%

Section: Hindgut Plasticity In Wallabies Fed Hay Either Unchopped or mentioning

confidence: 99%

Section: Hindgut Plasticity In Wallabies Fed Hay Either Unchopped or mentioning

confidence: 99%

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Hindgut Plasticity in Wallabies Fed Hay either Unchopped or Ground and Pelleted: Fiber Is Not the Only Factor

Munn

Clissold²,

Tarszisz³

et al. 2009

Physiological and Biochemical Zoology

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“…Total SCFA concentrations were lower during IBA and posthibernation than in summer, reflecting that at euthermic T b gut microbes are likely substrate limited due to host fasting. Other studies have reported low cecal SCFA concentrations in hibernators upon emergence from hibernation and slow increases through the early active season (4,42), suggesting that it requires considerable time (weeks) after ending hibernation for SCFA concentrations and molar proportions to rebound to summer levels. Interestingly, although at low concentrations at all sample periods, concentrations of BCFA were significantly higher during IBA and posthibernation than during torpor, indicative of increased mucin and protein catabolism (43) associated with high T b and a lack of dietary-derived nutrients.…”

Section: Discussionmentioning

confidence: 93%

Effects of Season and Host Physiological State on the Diversity, Density, and Activity of the Arctic Ground Squirrel Cecal Microbiota

Stevenson

Duddleston

Buck

2014

Appl Environ Microbiol

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We examined the seasonal changes of the cecal microbiota of captive arctic ground squirrels (Urocitellus parryii) by measuring microbial diversity and composition, total bacterial density and viability, and short-chain fatty acid concentrations at four sample periods (summer, torpor, interbout arousal, and posthibernation). Abundance of Firmicutes was lower, whereas abundances of Bacteroidetes, Verrucomicrobia, and Proteobacteria were higher during torpor and interbout arousal than in summer. Bacterial densities and percentages of live bacteria were significantly higher in summer than during torpor and interbout arousal. Likewise, total short-chain fatty acid concentrations were significantly greater during summer than during torpor and interbout arousal. Concentrations of individual short-chain fatty acids varied across sample periods, with butyrate concentrations higher and acetate concentrations lower during summer than at all other sample periods. Characteristics of the gut community posthibernation were more similar to those during torpor and interbout arousal than to those during summer. However, higher abundances of the genera Bacteroides and Akkermansia occurred during posthibernation than during interbout arousal and torpor. Collectively, our results clearly demonstrate that seasonal changes in physiology associated with hibernation and activity affect the gut microbial community in the arctic ground squirrel. Importantly, similarities between the gut microbiota of arctic ground squirrels and thirteen-lined ground squirrels suggest the potential for a core microbiota during hibernation.A lthough gut microbes share a mutualistic relationship with their mammalian hosts in which they benefit from access to fermentable substrates and a suitable living environment (1), the gut microbiota may be exposed to periods of little or no available dietary polysaccharides when the host is fasting. Extended periods of host fasting likely select for microbes that are able to degrade and subsist on host-derived substrates such as mucins and other glycoproteins (2-4). Indeed, several studies have revealed a profound effect of fasting on the gut microbiota. For example, fasting Burmese pythons (Python molurus) have higher relative abundances of Bacteroidetes, a phylum with species able to utilize hostderived substrates (1), whereas greater relative abundances of Firmicutes, which rely upon diet-derived substrates (5), were observed after the ingestion of a meal (6). Similarly, fasted Syrian hamsters (Mesocricetus auratus) exhibit decreased bacterial densities, relative abundance of Firmicutes, and microbial metabolic activity compared to those of fed hamsters (7).Many obligate seasonal hibernators (e.g., ground squirrels) naturally exhibit an endogenous circannual rhythm of hibernation and activity (reviewed in reference 8). During hibernation, animals voluntarily fast, and they conserve endogenous energy reserves by entering a state of torpor characterized by days to weeks of profoundly reduced metabolic rate, body temper...

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“…In the weeks prior to the onset of hibernation, obligate hibernators decrease rates of feeding and activity (28)(29)(30). Reduced feeding correlates with changes in gastrointestinal tract (GIT) physiology (29) that occur prior to hibernation in alpine marmots (Marmota marmota) and thirteen-lined ground squirrels (31,32). It is possible that the decreased metabolic rate (33) and decreased body temperature (T b ) (34) in arctic ground squirrels are reflective of reduced feeding and changes in the gut and gut microbiota in preparation for the onset of hibernation.…”

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confidence: 99%

Temporal Dynamics of the Cecal Gut Microbiota of Juvenile Arctic Ground Squirrels: a Strong Litter Effect across the First Active Season

Stevenson

Buck

Duddleston

2014

Appl Environ Microbiol

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Arctic ground squirrels (Urocitellus parryii) are active for a scant 3 to 5 months of the year. During the active season, adult squirrels compete for mates, reproduce, and fatten in preparation for hibernation, while juvenile squirrels, weaned in early July, must grow and acquire sufficient fat to survive their first hibernation season. During hibernation, the gut microbial community is altered in diversity, abundance, and activity. To date, no studies have examined the gut microbiota of hibernators across the truncated active season. We characterized trends in diversity (454 pyrosequencing), density (flow cytometry), viability (flow cytometry), and metabolism (short-chain fatty acid analysis) of the gut microbial community of juvenile arctic ground squirrels across their first active season at weaning and at 4, 6, 8, and 10 weeks postweaning. At 8 weeks postweaning, the mean bacterial density was significantly higher than that at weaning, and the mean percentage of live bacteria was significantly higher than that at either weaning or 4 weeks postweaning. No significant differences in microbial diversity, total short-chain fatty acid concentrations, or molar proportions of individual short-chain fatty acids were observed among sample periods. The level of variability in gut microbial diversity among squirrels was high across the active season but was most similar among littermates, except at weaning, indicating strong maternal or genetic influences across development. Our results indicate that genetic or maternal influences exert profound effects on the gut microbial community of juvenile arctic ground squirrels. We did not find a correlation between host adiposity and gut microbial diversity during prehibernation fattening, likely due to a high level of variability among squirrels.

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Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots ( Marmota marmota )

Cited by 86 publications

References 37 publications

Hindgut Plasticity in Wallabies Fed Hay either Unchopped or Ground and Pelleted: Fiber Is Not the Only Factor

Hindgut Plasticity in Wallabies Fed Hay either Unchopped or Ground and Pelleted: Fiber Is Not the Only Factor

Effects of Season and Host Physiological State on the Diversity, Density, and Activity of the Arctic Ground Squirrel Cecal Microbiota

Temporal Dynamics of the Cecal Gut Microbiota of Juvenile Arctic Ground Squirrels: a Strong Litter Effect across the First Active Season

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