Gross intestinal morphometry and allometry in primates

Although it is generally assumed that among mammals and within mammal groups, those species that rely on diets consisting of greater amounts of plant fiber have larger gastrointestinal tracts (GIT), statistical evidence for this simple claim is largely lacking. We compiled a dataset on the length of the small intestine, caecum, and colon in 42 strepsirrhine, platyrrhine, and catarrhine primate species, using specimens with known body mass (BM). We tested the scaling of intestine length with BM, and whether dietary proxies (percentage of leaves and a diet quality index) were significant covariates in these scaling relationships, using two sets of models: one that did not account for the phylogenetic structure of the data, and one that did. Intestine length mainly scaled geometrically at exponents that included 0.33 in the confidence interval; Strepsirrhini exhibited particularly long caeca, while those of Catarrhini were comparatively short. Diet proxies were only significant for the colon and the total large intestine (but not for the small intestine or the caecum), and only in conventional statistics (but not when accounting for phylogeny), indicating the pattern occurred across but not within clades. Compared to terrestrial Carnivora, primates have similar small intestine lengths, but longer large intestines. The data on intestine lengths presented here corroborate recent results on GIT complexity, suggesting that diet, as currently described, does not exhaustively explain GIT anatomy within primate clades.     

Mammalian intestinal allometry,phylogeny, trophic level and climate

An often-stated ecomorphological assumption that has the status of ‘textbook knowledge’ is that the dimensions of the digestive tract correlate with diet, where herbivores—consuming diets of lower digestibility—have longer intestinal tracts than faunivores—consuming diets of higher digestibility. However, statistical approaches have so far failed to demonstrate this link. Here, we collated data on the length of intestinal sections and body mass of 519 mammal species, and test for various relationships with trophic, climatic and other biological characteristics. All models showed a strong phylogenetic signal. Scaling relationships with body mass showed positive allometry at exponents greater than 0.33, except for the caecum, which is particularly large in smaller species. Body mass was more tightly linked to small intestine than to large intestine length. Adding a diet proxy to the relationships increased model fit for all intestinal sections, except for the small intestine when accounting for phylogeny. Thus, the diet has a main effect on the components of the large intestine, with longer measures in herbivores. Additionally, measures of habitat aridity had a positive relationship with large intestine length. The small intestine was longer in species from colder habitats at higher latitudes, possibly facilitating the processing of peak intake rates during the growing season. This study corroborates intuitive expectations on digestive tract anatomy, while the dependence of significant results on large sample sizes and inclusion of specific taxonomic groups indicates that the relationships cannot be considered fixed biological laws.     

Comparative omasum anatomy in ruminants: Relationships with natural diet,digestive physiology,and general considerations on allometric investigations

The omasum is the third forestomach compartment of pecoran ruminants. It is assumed that the re-absorption of fluid present in the forestomach digesta (that facilitates particle sorting, digestion, and harvest of microbes) is its main function, so that less diluted digesta is submitted to enzymatic digestion in the lower digestive tract. Here, we evaluate measures of omasum size (representing 84 ruminant species in the largest data set) against body mass and proxies of the natural diet (%grass) or forestomach physiology (fluid throughput), using phylogenetically controlled models. The origin of specimens (free-ranging or captive) did not have an effect in the data set. Models with the best support invariably either included %grass or a physiology proxy in addition to body mass. These effects were not necessarily additive (affecting the intercept of the allometric regression), but often indicated a change in the allometric body mass-exponent with diet or physiology. Only models that allowed an influence on the allometric exponent yielded basic exponents compatible with predictions derived from geometry. Species that include more grass in their natural diet, or that have a “cattle-type” physiology marked by a high forestomach fluid throughput, generally have larger omasa. However, the existence of outliers, as well as the overall data pattern, suggest that this is not an obligatory morphophysiological condition. Circumstantial evidence is presented leading to the hypothesis that the comparatively small and less complex omasa of “moose-type” species do not necessarily represent an “original” state, but may be derived from more complex states by ontogenetic reduction and fusion of omasal laminae.     

Herbivory and Body Size: Allometries of Diet Quality and Gastrointestinal Physiology,and Implications for Herbivore Ecology and Dinosaur Gigantism

Digestive physiology has played a prominent role in explanations for terrestrial herbivore body size evolution and size-driven diversification and niche differentiation. This is based on the association of increasing body mass (BM) with diets of lower quality, and with putative mechanisms by which a higher BM could translate into a higher digestive efficiency. Such concepts, however, often do not match empirical data. Here, we review concepts and data on terrestrial herbivore BM, diet quality, digestive physiology and metabolism, and in doing so give examples for problems in using allometric analyses and extrapolations. A digestive advantage of larger BM is not corroborated by conceptual or empirical approaches. We suggest that explanatory models should shift from physiological to ecological scenarios based on the association of forage quality and biomass availability, and the association between BM and feeding selectivity. These associations mostly (but not exclusively) allow large herbivores to use low quality forage only, whereas they allow small herbivores the use of any forage they can physically manage. Examples of small herbivores able to subsist on lower quality diets are rare but exist. We speculate that this could be explained by evolutionary adaptations to the ecological opportunity of selective feeding in smaller animals, rather than by a physiologic or metabolic necessity linked to BM. For gigantic herbivores such as sauropod dinosaurs, other factors than digestive physiology appear more promising candidates to explain evolutionary drives towards extreme BM.     

Unusual intestinal lamellae in the nematode Rhabditophanes sp. KR3021 (Nematoda: Alloinematidae)

The free-living nematode Rhabditophanes sp. has recently been placed in a clade of animal parasites and may be a unique example of a reversal to a nonparasitic lifestyle. Detailed morphological analysis of the intestine reveals the unusual and unique structure of splitting microlamellae forming a meshwork with cavities along the entire intestinal tract. Secretion vesicles were observed along the whole tract and along the length of the lamellae. It is suggested that these lamellae are adaptations to a different digestive strategy where low food availability and a low absorption surface are compensated for by maximizing the nutrient uptake efficiency along the entire length of the intestine. The likely reversal to a free-living life cycle may have caused drastic changes in diet, providing the necessary driving forces to such morphological changes.     

Morphological adaptations of the digestive tract of tropical cyprinids and cichlids to diet

Eight cyprinids with four different feeding habits fall into two distinct groups according to morphological adaptations of the intestine: (i) carnivorous and omnivorous cyprinids with large gut diameter and large mucosal surface which decreases from the foregut to the hindgut; (ii) benthivorous and phytoplanktivorous cyprinids with small gut diameter and small mucosal surface which is more or less uniformly built along the intestine, although relative gut length may vary considerably (1.45–6.10). Although the intestine of phytoplanktivorous cyprinids is extremely elongated, it appears less adapted for processing a refractory diet than that of cichlids with similar feeding habits.     

Convergence of macroscopic tongue anatomy in ruminants and scaling relationships with body mass or tongue length

Various morphological measures demonstrate convergent evolution in ruminants with their natural diet, in particular with respect to the browser/grazer dichotomy. Here, we report quantitative macroanatomical measures of the tongue (length and width of specific parts) of 65 ruminant species and relate them to either body mass (BM) or total tongue length, and to the percentage of grass in the natural diet (%grass). Models without and with accounting for the phylogenetic structures of the dataset were used, and models were ranked using Akaike's Information Criterion. Scaling relationships followed geometric principles, that is, length measures scaled with BM to the power of 0.33. Models that used tongue length rather than BM as a body size proxy were consistently ranked better, indicating that using size proxies that are less susceptible to a wider variety of factors (such as BM that fluctuates with body condition) should be attempted whenever possible. The proportion of the freely mobile tongue tip of the total tongue (and hence also the corpus length) was negatively correlated to %grass, in accordance with concepts that the feeding mechanism of browsers requires more mobile tongues. It should be noted that some nonbrowsers, such as cattle, use a peculiar mechanism for grazing that also requires long, mobile tongues, but they appear to be exceptions. A larger corpus width with increasing %grass corresponds to differences in snout shape with broader snouts in grazers. The Torus linguae is longer with increasing %grass, a finding that still warrants functional interpretation. This study shows that tongue measures covary with diet in ruminants. In contrast, the shape of the tongue (straight or “hourglass‐shaped” as measured by the ratio of the widest and smallest corpus width) is unrelated to diet and is influenced strongly by phylogeny. J. Morphol. 277:351–362, 2016. © 2015 Wiley Periodicals, Inc.     

Digestive enzymes in the germ-free animal

The digestive physiology of the germ-free animal has a number of characteristics (cecal hypertrophy, slower small intestine cell renewal, slower gastric emptying and intestinal transit) which distinguish it from that of the conventional animal. If the germ-free model is to be used to determine the role of gastrointestinal microflora in the nutrition of the conventional animal, it is essential to complete the study of these characteristics by data on digestive enzymes in the germ-free. The present paper analyzes these data. There is little information on salivary amylase and none on gastric proteolytic enzymes and intestinal peptidases. More complete data on exocrine pancreas enzymes and intestinal disaccharidases show that the digestive equipment is similar in germ-free and conventional animals. Bile salts, not considered as digestive enzymes, are qualitatively and quantitatively different, depending on the digestive tract bacterial environment. In general, the germ-free animal has some characteristics which should permit better utilization of the diet ingested. Measurements of apparent digestibility do not confirm this hypothesis since results obtained in germ-free and conventional animals of the same species are contradictory.     

Vasoactive intestinal polypeptidergic innervation and gastroenteropancreatic system: an immunocytochemical study in the hedgehog Erinaceus europaeus.

The pattern of the digestive vasoactive intestinal polypeptide (VIP)-ergic innervation is described immunohistochemically in the hedgehog Erinaceus europaeus. This animal is a small-sized, wild, nocturnal, lower eutherian mammal whose gastrointestinal tract shows some similarities with the avian gut. The myenteric plexus of the stomach, the mucosa of the small intestine and the circular muscle layer of the large intestine are the best VIP-innervated structures. The pattern of the positive innervation is similar to that described in other mammals and in some bird species. The widespread diffusion of the neuropeptide in the gut is probably due to the importance of its functions in the digestive physiology.     

蓝翅希鹛消化系统的初步研究

对6只(3♀,3♂)蓝翅希鹛的消化系统进行了解剖观察,结果表明:蓝翅希鹛的舌成细长三角形,雌、雄舌尖端差异显著:雌鸟舌尖端各有一根长刺毛,而雄鸟无此长刺毛;在舌前端正中央还有一"v"形的凹缺,使舌成二分叉,雌鸟分叉深约2.77 mm,雄鸟为1.63 mm。食道颈胸部分段不明显,食管长18.64~23.55 mm,嗉囊外观不明显。腺胃乳突短而小,分布均匀;肌胃发达,具角质膜。肠道长与体长基本相等,小肠较发达,雌鸟长100.90 mm,占肠道总长90.08%,雄鸟分别为102.52 mm和89.60%;具有双侧盲肠,但不发达,占肠道总长的2.3%~2.8%,右侧盲肠略大于左侧;直肠短,雌鸟仅占肠道8.55%,雄鸟占8.72%。肝为体内最大的消化腺,分左右两叶。胰位于十二指肠袢内,细长形,分二小叶。由消化道特征说明其食性是以食虫为主的杂食性鸟类。     

Multiple pathways from three types of sugar receptor sites to metabotropic transduction pathways of the blowfly: study by the whole cell-clamp experiments

Differences in the allometric scaling between gut capacity (with body mass, BM^1.00) and food intake (with BM^0.75) should theoretically result in a scaling of digesta retention time with BM^0.25 and therefore a higher digestive efficiency in larger herbivores. This concept is an important part of the so-called ‘Jarman–Bell principle’ (JBP) that explains niche differentiation along a body size gradient in terms of digestive physiology. Empirical data in herbivorous mammals, however, do not confirm the scaling of retention time, or of digestive efficiency, with body mass. Here, we test these concepts in herbivorous reptiles, adding data of an experiment that measured food intake, digesta retention, digestibility and gut capacity in 23 tortoises (Testudo graeca, T. hermanni , Geochelone nigra, G. sulcata, Dipsochelys dussumieri) across a large BM range (0.5–180 kg) to a literature data collection. While dry matter gut fill scaled to BM^1.07 and dry matter intake to BM^0.76, digesta mean retention time (MRT) scaled to BM^0.17; the scaling exponent was not significantly different from zero for species > 1 kg. Food intake level was a major determinant of MRT across reptiles and mammals. In contrast to dietary fibre level, BM was not a significant contributor to dry matter digestibility in a General Linear Model. Digestibility coefficients in reptiles depended on diet nutrient composition in a similar way as described in mammals. Although food intake is generally lower and digesta retention longer in reptiles than in mammals, digestive functions scale in a similar way in both clades, indicating universal principles in herbivore digestive physiology. The reasons why the theoretically derived JBP has little empirical support remain to be investigated. Until then, the JBP should not be evoked to explain niche differentiation along a body size axis in terms of digestive physiology.     

蜂桶寨自然保护区中华姬鼠和社鼠食性的季节变化及与肠道长度的关系

为揭示啮齿动物食性及其对消化道肠道长度的影响,我们于2008 年在四川省宝兴县蜂桶寨国家级自然保护区内以中华姬鼠和社鼠为对象展开了研究。结果发现社鼠和中华姬鼠均以摄食种子为主,食谱中各食物成分在性别之间无显著差异,但季节变化明显。在各食物成分中,摄入种子百分比与中华姬鼠及社鼠小肠长之间呈显著正相关,而昆虫成分则相反。分析认为,中华姬鼠和社鼠取食食物成分的季节变化,可能与不同季节中食物资源可获得性的不同有关,消化道长度的变化可能体现了对季节性食物资源和能量需求的适应.     

灰胸薮鹛消化系统形态的初步研究

对灰胸薮鹛（Liocichla omeiensis）消化系统的形态学作了初步观察,结果表明,灰胸薮鹛舌前端有刺毛状结构,后端有一排尖端后指的栉状突,且中间小两边大;雄鸟在舌前端正中央还有一“v”形的凹缺,深约2．5mm;雌鸟食道颈段长为13．2mm,雄鸟为17．5mm;嗉囊雌鸟长7．5mm,雄鸟长8．4mm;食道胸段雌鸟长15．5mm,雄鸟长14．7mm;肌胃发达,具角质膜,腺胃乳突短而小;肠道长与体长基本相等,小肠较发达,雌鸟长153．7mm,占肠道总长92．6％,雄鸟为133mm和95％,具有双侧盲肠,占肠道总长的3．3％,大肠短,雌鸟仅占肠道7．5％,雄鸟仅占4．75％;肝为体内最大的消化腺,分左右两叶;胰位于十二指肠袢内,细长形,分三小叶。     

Intestinal length of three California pinniped species

Forty-eight intestinal tracts, extracted from both sexes of California sea lions, Harbour seals and Northern elephant seals, were measured. The majority of intestinal tracts were removed from stranded animals that died from various causes. The sea lions and elephant seals, approximately equal in size, were larger than the Harbour seals. All species possess a small intestine which is significantly longer than even the entire gastrointestinal tract of herbivores of comparable size. Elephant seal small intestines, averaging approximately 25 times the seal's body length, were considerably longer than the small intestines of either sea lions (averaged more than 18 times the body length) or Harbour seals (averaged nearly 16 times the body length). However, the large intestines of elephant seals were shorter than either of the other two species. Among the sea lions and Harbour seals the large intestines were approximately equal in length. Sea lions and Harbour seals also showed a close correlation between standard length and total intestinal length. Among elephant seals these two parameters showed greater variability. The functional significance of the extremely long small intestine remains unclear. Certainly, the large body mass and high energy requirements of these animals has contributed to the development of a long intestinal tract. It also appears likely that diet and the high motility rate of digesta influenced the intestinal development. Comparatively, the significantly shorter large intestine of elephant seals probably relates to this species' remarkable capabilities in water conservation and metabolic water retention.     

How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals?

Summary What digestive adaptations permit herbivorous nonruminant mammals to sustain much higher metabolic rates than herbivorous lizards, despite gross similarity in digestive anatomy and physiology? We approached this question by comparing four herbivorous species eating the same diet of alfalfa pellets: two lizards (chuckwalla and desert iugana) and two mammals (desert woodrat and laboratory mouse). The mammals had longer small and large intestines, greater intestinal surface area, much higher (by an order of magnitude) food intake normalized to metabolic live mass, and much faster food passage times (a few hours instead of a few days). Among both reptiles and mammals, passage times increase with body size and are longer for herbivores than for carnivores. The herbivorous lizards, despite these much slower passage times, had slightly lower apparent digestive efficiencies than the mammals. At least for chuckwallas, this difference from mammals was not due to differences in body temperature regime. Comparisons of chuckwallas and woodrats in their assimilation of various dietary components showed that the woodrat's main advantage lay in greater assimilation of the dietary fiber fraction. Woodrats achieved greater fiber digestion despite shorter residence time, but possibly because of a larger fermentation chamber, coprophagy, and/or different conditions for microbial fermentation. We conclude with a comparative overview of digestive function in herbivorous lizards and mammals, and with a list of four major unsolved questions.     

黑斑侧褶蛙消化道重量及长度的性别和季节差异

消化道是联系脊椎动物能量摄入和能量支出之间关系的纽带,其重量和长度对外界环境具有高度的敏感性和弹性(flexibility)。以黑斑侧褶蛙(Pelophylax nigromaculata)为研究对象,测定了山东聊城地区2012年夏季(16只,8♀/8♂)、秋季(19只,9♀/10♂)及翌年春季(17只,8♀/9♂)其体重、体长、胴体湿重和干重系数、总消化道及各段(食道、胃、小肠和大肠)的湿重、干重和长度系数的性别和季节差异(双因素方差分析),对有性别差异的指标,用单因素方差分析分别比较了雌、雄蛙的季节差异。结果显示,1)雌蛙的体重、体长均高于雄蛙,都在秋季最高,春季或夏季最低;雄蛙的胴体湿重系数高于雌蛙,夏季高于秋季;胴体干重系数既无性别差异,也无季节差异。2)除食道湿重系数无性别差异外,雌蛙总消化道及各段的湿重系数均高于雄蛙;除胃湿重系数无季节差异外,春季或秋季的总消化道及各段的湿重系数都高于夏季;雌蛙的总消化道干重和胃干重系数高于雄蛙,食道、小肠和大肠的干重系数无性别差异,所有的干重系数均无季节性差异。3)除雌蛙的大肠长系数高于雄蛙外,总消化道及各段的长度系数均无性别差异,春季和秋季的总消化道长、食道长及胃长系数均高于夏季,小肠长和大肠长系数均无季节性差异。结果表明,随着季节更替,黑斑侧褶蛙消化道各段的重量和长度表现出一定的弹性特征,这与各器官的功能及其生活环境的多样性是相适应的。     

Changes in the small intestine of Schistosoma mansoni-infected mice fed a high-fat diet

The consumption of a high-fat diet modifies both the morphology of the small intestine and experimentally tested effects of schistosomiasis mansoni. However, whether a schistosomiasis infection associated with a high-fat diet causes injury to the small intestine has never been investigated. Mice were fed either a high-fat or a standard-fat diet for 6 months and were then infected with Schistosoma mansoni cercariae. Physical characteristics of the intestinal tissue (mucosal thickness, small intestinal villi length and height, and abundance of goblet cells and enterocytes on the villous surface) and the distribution of granulomas along the intestinal segments and their developmental stage were measured at the time of sacrifice (9 or 17 weeks post-infection). The group fed a high-fat diet exhibited different granuloma stages, whereas the control group possessed only exudative granulomas. The chronically infected mice fed a high-fat diet exhibited higher granuloma and egg numbers than the acutely infected group. Exudative, exudative/exudative-productive and exudative-productive granulomas were present irrespective of diet. Computer-aided morphometric analysis confirmed that villus length, villus width, muscular height and submucosal height of the duodenal and jejunal segments were affected by diet and infection. In conclusion, a high-fat diet and infection had a significant impact on the small intestine morphology and morphometry among the animals tested.     

Phenotypic flexibility in the intestinal enzymes of the African clawed frog Xenopus laevis

The intestinal plasticity of digestive enzymes of amphibian species is poorly known. The goal of this study was to characterize digestive enzyme profiles along the small intestine of adult frogs, Xenopus laevis, in response to an experimental diet. We acclimated adult X. laevis for 30 days either to carbohydrate-rich or protein-rich diets, and determined the morphology and digestive enzymes of the small intestine. We found a significant difference of aminopeptidase-N activity between carbohydrate-rich and protein-rich acclimated animals. We also found a little variation in the expression of maltase activity, which contrast with the proposed hypothesis about the existence of digestive tradeoff in vertebrates. This finding supports the adaptive modulation hypothesis and suggests that caution is called for when analyzing physiological data regarding assumed discrete trophic category of species.     

Paracellular nutrient absorption in a gum-feeding new world primate, the common marmoset Callithrix jacchus

The common marmoset is one of the few callitrichid species that is not threatened or endangered in the wild, and is widely used in biomedical research, yet relatively little is understood about its digestive physiology. Dietary specialization on plant exudates has lead to relatively reduced small intestines, yet the common marmoset has exceptional dietary breadth, allowing it to successfully utilize a variety of habitats. We predicted that passive, paracellular nutrient absorption would be used by the common marmoset to a greater extent than in other non-flying mammals. We measured the bioavailability and rates of absorption of two metabolically inert carbohydrates not transported by mediated pathways (L-rhamnose and cellobiose, molecular masses of 164 and 342, respectively) to measure paracellular uptake, and of a non-metabolized D-glucose analog (3-O-methyl-D-glucose) to measure total uptake by both mediated and paracellular pathways. We found high bioavailability of 3-O-methyl-D-glucose (83+/-5%), and much higher bioavailability of the paracellular probes than in similarly sized non-flying mammals (30+/-3% and 19+/-2% for L-rhamnose and cellobiose, respectively). Passive, paracellular nutrient absorption accounts for around 30% of total glucose absorption in common marmosets and intestinal permeability is significantly higher than in humans, the only other species of primate measured to date. This may allow the common marmoset to maintain high digestive efficiency when feeding on higher quality foods (fruit, arthropods, gums with higher proportions of simple sugars), in spite of relatively reduced small intestines correlated with adaptations for fermentative digestion of plant gums. We find no evidence to support, in primates, the hypothesis that reliance on paracellular nutrient absorption should increase with body size in mammals, but suggest instead that it may be associated with small body size and/or taxon-specific adaptations to diet.     

A comparative study of digestion in North Atlantic seabirds

We present data on digestive efficiencies and gut retention times of eight North Atlantic seabird species, fed on two fish species – lesser sandeel Ammodytes marinus and whiting Merlangius merlangus – which commonly occur in the diet of wild seabirds. In an interspecific comparison, there was a positive relationship between retention time and digestive efficiency, which we suggest represents a trade-off between conflicting benefits of efficient digestion and rapid digestion. Analysis of excretion curves revealed that retention time of digesta in the stomach was more important than passage time of digesta through the intestine in determining whole gut retention time. Differences in stomach retention time of lesser sandeel and whiting explained the longer overall retention time of the latter diet. Stomach retention time and whole gut retention time were greater in species with relatively large stomachs, while intestine passage time was correlated with relative intestine length. Species which typically eat a wide range of food types, including low quality items, tended to have slow and efficient digestion and heavy stomachs, whereas species which specialise on readily digestible and energy dense food types had the opposite digestion strategy.