Latitudinal trends in digestive flexibility: testing the climatic variability hypothesis with data on the intestinal length of rodents

Flexibility of digestive features can be understood considering the benefits of digestion, which links animal foraging to metabolizable energy and nutrient gain, and its costs, which are partly indexed by digestive tract tissue mass, one of the most expensive to maintain in terms of energy and protein metabolism. In this article, we applied a meta-analytical approach to current data on rodents' small intestine length flexibility to evaluate the climatic variability hypothesis (CVH). This hypothesis states the following: (1) as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should be more flexible to persist at a site; (2) the greater phenotypic flexibility allows species to occupy more habitats and to become more widely distributed. We compiled data from 25 articles, which provided a total of 86 estimations of flexibility involving 20 rodent species. Consistent with CVH predictions, we found a positive correlation between small intestine length flexibility and latitude and between small intestine length flexibility and the number of habitats occupied by different species. When seen from the perspective of digestive physiology, our analysis is an important piece of evidence on the adaptive value of digestive flexibility in small mammals.     

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。     

Does diet variation determine the digestive tract length of Capoeta banarescui Turan,Kottelat, Ekmekci and Imamoglu, 2006?

This study tested the spatial variations in the digestive/intestine tract length of Capoeta banarescui, with regard to their diets in different habitats. Highly varied diets observed in a previous study within the same river system posed the question whether this flexibility is reflected in the digestive tract and intestine length of the species in the Ye?il?rmak River, Turkey. Totals of 382 specimens (standard length 4.6–19.1 cm) were captured by electro‐fishing along the river in September 2012 at 11 locations spanning elevations from 34 to 992 m. The stomach, intestine and total digestive tract lengths were measured, and stomach contents analysed from 196 specimens. For statistical analyses, the stomach, intestine and total digestive tract length were expressed as percentages of total weight and standard length. The data provided evidence that the digestive tract and intestine lengths varied significantly among locations in association with the diet. Fish having dominantly carnivorous diets (e.g. chironomid larvae/invertebrates) in two locations had significantly shorter intestines and digestive tracts than those with diets dominated by benthic algae and other plants. The data indicated that C. banarescui showed broad flexibility in their feeding habits. Feeding heavily on plant materials might lead to the development of longer digestive tracts, increasing the active surface area for digestion; alternatively, there may be less invested in development of the digestive tract when feeding primarily on carnivorous diets where the respective digestive enzymes are readily available. The data suggest that phenotypic plasticity in the digestive tract length of C. banarescui is associated more with the abundant protein‐rich carnivorous food sources in the studied habitats. Whether this digestive tract plasticity has a genetic background remains to be verified in future studies.     

Seed dispersal potential by wild mallard duck as estimated from digestive tract analysis

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Effect of ambient temperature and energy demands on digestive functions in leaf-eared mice (Phyllotis darwini) from central Chile

 The leaf-eared mouse, Phyllotis darwini, is a nocturnal rodent inhabiting the semiarid and Mediterranean habitats of northern and central Chile. Previous observations suggested that in the field, individuals may change food intake according to seasonal changes in ambient temperature. We therefore anticipated that P. darwini should increase food intake in response to lower ambient temperature. As predicted, results of food trials and digestive measurements demonstrated that P. darwini increases food intake and assimilation at lower ambient temperatures but does not increase food mean retention time. At lower ambient temperatures, individuals increase digestive tract size thus improving body mass maintenance and perhaps survival during winter. Received 17 June 1996 / Revised: 25 February 1997 / Accepted: 13 March 1997     

温度和光周期驯化对树麻雀消化道形态特征和能量预算的影响

为探讨温度和光周期驯化对树麻雀消化道形态特征和能量预算的影响,以不同环境温度(5℃和25℃)、不同光周期(16L∶8D和8L∶16D)的4组树麻雀进行为期4周的人工气候箱驯化,并对驯化后的4组树麻雀消化道形态特征各指标以体质量为协变量,采用温度、光周期双因素协方差分析和组间进行单因素协方差分析及进行Tukey HSD比较。结果表明,温度降低或光周期缩短导致消化道长度极显著增加;反之,则缩短。温度显著影响消化道干组织质量;温度和光周期的交互作用对消化道净鲜质量和干组织质量的影响显著;总消化道和各器官的长度(直肠长度除外)、质量均存在明显的组间差异。可见,不同的温度或光周期可引起树麻雀消化道形态结构和功能能力相应的适应性变化,消化道各器官长度和质量的改变与其个体的摄能需求密切相关,消化道各器官功能能力和器官能耗之间高投资高收益的能量预算是个体适合度与环境压力之间能量预算的结果。     

Ecological and Geographical Reasons for the Variation of Digestive Tract Length in Anurans

Changes of environmental conditions can shape organs size evolution in animal kingdoms. In particular, environmental changes lead to difference in food resources between different habitats, thereby affecting individual's energy intake and allocation. The digestive theory states that animals consuming food with low contents of digestible materials should result in increasing gut length. In this study, to test the hypothesis of digestive theory, we studied ecological and geographical reasons for variation in digestive tract length among 35 species of anurans distributing in different altitude and latitude. The results showed that ecological type significantly affected digestive tract length among species, with aquatic and terrestrial species having longer digestive tract than arboreal ones. Latitude was positively correlated with digestive tract length. However, altitude, as well as monthly mean temperature and precipitation, did not correlate with digestive tract length among species. Our findings suggest that aquatic and terrestrial species might forage less digestible materials than arboreal species, thereby displaying relatively longer digestive tract than arboreal species.     

Do changes in dietary chemistry during ontogeny affect digestive performance in adults of the herbivorous rodent Octodon degus?

We characterize the flexibility in digestive performance in degus (Octodon degus) an herbivorous rodent. We tested the hypothesis that dietary and physiological-digestive flexibility are correlated. Degus were fed with artificial diets of different chemical composition from weaning to adulthood and their digestive performance was measured through records of apparent digestibility. The starch content of the acclimation diet was not correlated with protein digestibility nor was it correlated with starch digestibility. In addition, digestive tract morphology was not affected by dietary treatments. Hence, an absence of morphological and physiological flexibility related to digestive traits was observed in degus. The lower flexibility in digestive performance given by our dietary experimental treatments of degus, may be an evolutionary constraint related to their specialized herbivorous food habits.     

Dietary Flexibility and Feeding Strategies of <Emphasis Type="Italic">Eulemur</Emphasis>: A Comparison with <Emphasis Type="Italic">Propithecus</Emphasis>

Despite the great variety of habitats in Madagascar, Eulemur has successfully populated most forested habitats on the island. Although the high dietary flexibility of Eulemur is often credited as one of the drivers of its evolutionary success, other behavioral evidence suggests a limited capacity for dietary switching. To shed light on the feeding strategies of Eulemur, we compared the dietary flexibility between populations of this genus with that of another widespread lemur taxon, Propithecus. We hypothesized that Eulemur would show greater dietary flexibility than Propithecus, which has a digestive system specialized for folivory, and that Eulemur living in dry forests would switch its diet from fruit to other food seasonally. To examine these hypotheses, we performed a phylogenetic least-squares analysis on 10 populations of Eulemur and 7 of Propithecus to assess the contribution of environmental variables and body mass on their dietary flexibility while controlling for phylogenetic relatedness. Eulemur relied heavily on fruit and did not show large variations in primary food over the year. Propithecus consumed leaves and fruits equally and exhibited considerable flexibility across seasons. Therefore, in contrast to our predictions, the anatomical specialization for fiber digestion heightens dietary flexibility in Propithecus. At the intrageneric level, we found similar ecogeographic variation; populations of both genera with heavier body mass consumed more fruit. As we predicted, Eulemur in drier habitats switched the diet from fruit to alternative food more frequently. To compensate for low dietary flexibility, Eulemur mostly adopts a power-feeding strategy by which it increases energy expenditure to acquire patchily distributed fruit resources.     

Latitudinal patterns in rodent metabolic flexibility

Macrophysiology is defined as the study of variation in physiological traits-including physiological trait flexibility-over large geographical and temporal scales, and the ecological implications of this variation. A classic example of a macrophysiological trend is the one emerging from the climatic variability hypothesis, which states that as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should be more plastic than individuals inhabiting lower latitudes. In this context, we evaluate the correlation between absolute metabolic scope during cold exposure (an instantaneous measure of metabolic flexibility) and different geographic and climatic variables for 48 rodent species. Conventional and phylogenetic informed analyses indicated a positive correlation between metabolic scope and geographic latitude. These findings, together with previous reports on latitudinal pattern in phenotypic flexibility, suggest that an increase in physiological flexibility with latitude may hold for many phenotypic traits.     

Within-species digestive tract flexibility in rufous-collared sparrows and the climatic variability hypothesis

The climatic variability hypothesis (CVH) states that species are geographically more widespread at higher latitudes because individuals have a broader range of physiological tolerance or phenotypic flexibility as latitude and climatic variability increase. However, it remains unclear to what extent climatic variability or latitude, acting on the phenotype, account for any observed geographical gradient in mean range size. In this study, we analyzed the physiological flexibility within the CVH framework by using an intraspecific population experimental approach. We tested for a positive relationship between digestive-tract flexibility (i.e., morphology and enzyme activities) and latitude and climatic and natural diet variability in populations of rufous-collared sparrows (Zonotrichia capensis) captured in desert (27°S), Mediterranean (33°S), and cold-temperate (41°S) sites in Chile. In accordance with the CVH, we observed a positive relationship between the magnitude of digestive-tract flexibility and environmental variability but not latitude. The greatest digestive flexibility was observed in birds at middle latitudes, which experience the most environmental variability (a Mediterranean climate), whereas individuals from the most stable climates (desert and cold-temperate) exhibited little or no digestive-tract flexibility in response to experimental diets. Our findings support the idea that latitudinal gradients in geographical ranges may be strongly affected by the action of regional features, which makes it difficult to find general patterns in the distribution of species.     

Optimal feeding strategy of the temperate herbivorous fish Aplodactylus punctatus: the effects of food availability on digestive and reproductive patterns

In this study we examined differences in feeding behevior of populations of the marine temperate herbivorous fish Aplodactylus punctatus, in three different localities off the Chilean coast, which differ qualitatively and quantitatively in food availability. We test whether food selection follows optimal foraging strategics, whether there is any modification of the fishes' digestive tracts in relation to their diets, and whether differences in diet quality affect the allocation of energy into reproduction and maintenance in these populations. Samples of this fish and of the understore algal assemblages were taken seasonally from May 1989 to February 1990. For each population we analyzed dietary composition, weight of the digestive tract and of the food content, the condition factor (K), and the gonadosomatic index (GSI). Our results showed that the diet observed in the three populations closely resembled the differences in macro-algal abundance and composition among the three localities studied. Local differences in diet quality were inversely related to the amount of food consumption and size of the digestive tract, suggesting that under differential conditions of food availability A. punctatus is able to compensate for variations in food quality through a flexibility in its digestive strategies. The nutritional status (K) of individuals, and their reproductive pattern (GSI) were directly related to diet quality. These results indicate that although A. punctatus is able to adjust its digestive processes to different algal food regimes, the digestive modifications observed in food-poor environments are not sufficient to compensate for the lack of food and allow fish to reach the nutritional status and reproductive output reached in a food-rich environment. This study represents the first natural experiment demonstrating a direct relationship among food availability, feeding patterns, digestive processes, and reproductive effort.     

Digestive tract morphology and digestion in the wombats (Marsupialia: Vombatidae)

Summary Wombats consume grasses and sedges which are often highly fibrous. The morphology of the digestive tract and the sequence of digestion were studied in two species of wombats from contrasting habitats: Vombatus ursinus from mesic habitats and Lasiorhinus latifrons from xeric regions. Studies were performed on wild wombats consuming their natural winter diets, and on captive wombats fed a high-fibre pelleted straw diet. Vombatus had a shorter digestive tract (9.2 vs 12.5 times body length) of greater capacity (wet contents 17.9 vs 13.7% body weight) than Lasiorhinus. The most capacious region of the digestive tract was the proximal colon (62–79% of contents). The proportional length and surface area of the proximal colon were greater in Vombatus, but those of the distal colon were greater in Lasiorhinus. These digestive morphologies may reflect adaptations for greater capacity and longer retention of digesta in Vombatus, but greater absorption and lower faecal water loss in Lasiorhinus. Apparent digestion along the digestive tract was estimated by reference to lignin. The proximal colon was the principal site of fibre and dry matter digestion, whereas nitrogen was mainly digested in the small intestine. Depot fats in captive wombats were highly unsaturated and reflected those in the diet. Therefore, lipids, proteins and soluble carbohydrates in the plant cell contents were digested and absorbed in the stomach and small intestine. Conversely, dietary fibre was probably retained and digested by microbial fermentation along the proximal colon.Abbreviations ADF acid detergent fibre - DM dry matter - NDF neutral detergent fibre - SD standard deviation     

Plasticity in food assimilation,retention time and coprophagy allow herbivorous cavies (Microcavia australis) to cope with low food quality in the Monte desert

Energy balance depends on the efficiency with which organisms make use of their trophic resources, and has direct impact on their fitness. There are environmental variations that affect the availability as well as the quality of such resources; energy extraction also depends on the design of the digestive tract. It is expected that features associated with food utilization will be subjected to selective pressures and show some adjustment to the variability of the environment. Since energetic constraints challenge animals to display digestive compensatory mechanisms, the objective of this study is to determine the physiological and behavioral responses to spatial and seasonal heterogeneity in food quality. We investigated digestive strategies (digestive efficiency and coprophagy) in cavies inhabiting two different populations, and hence naturally experiencing different levels of diet quality. Cavies under experimentally different quality diets showed changes in dry matter digestibility and intake, digesta retention time and coprophagy. Our results partially support the expectations from theory and also reveal interpopulation differences in the ability to cope with changes in food quality, and may explain the capability of Microcavia australis to colonize extreme habitats.     

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.     

Gut length plasticity in perch: into the bowels of resource polymorphisms

Resource polymorphisms, intraspecific variation in morphology due to differential resource use, are common across a wide range of animal taxa. The focus in studies of such polymorphisms has been on external morphology, but the differential use of food resources could also influence other phenotypic traits such as the digestive performance. In the present study, we experimentally demonstrate that Eurasian perch ( Perca fluviatilis L.) display adaptive plasticity in gut length when exposed to different food types. Perch fed a less digestible food type developed relatively longer guts compared to fish fed a more easily digested food type. This divergence in gut length was also apparent under natural conditions because perch inhabiting the littoral and pelagic habitats of a lake differed in resource use and relative gut length. Despite that the digestive system in perch is plastic, we found that individuals switching to a novel food type might experience an initial fitness cost of the diet switch in the form of a temporary reduction in body condition. These results show the importance of gut length plasticity for an ontogenetic omnivore but also a cost that might prevent diet switching in polymorphic populations.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 517–523.     

Altitudinal Variation in Digestive Tract Lengh in Feirana quadranus

Selective pressures favor variation in organ size in response to environmental changes and evolutionary process. In particular, changes in environmental temperature and rainfall at different altitudes often affect food resources, thereby mediating energy intake and allocation. The digestive tract provided a functional relationship between energy intake and allocation, of which gut morphology was associated with diet changes and food quality under different environments. Here we studied altitudinal variation in the digestive tract across four Feirana quadranus populations and tested the hypothesis that relative size of digestive tract should increase with increasing altitude. The results showed that although significant variation in length of the digestive tract was observed in females among populations, altitudinal variation in relative length of digestive tract or gut was non-significant. In addition, the digestive tract length was not correlated with temperature and precipitation across the four populations. Our findings suggest that individuals living in low-temperature and-precipitation populations at high altitudes did not display longer digestive tract than high temperature and precipitation populations at low altitudes, possibly because of small populations or sample sizes.     

Phenotypic and genetic divergence among harbour porpoise populations associated with habitat regions in the North Sea and adjacent seas

Determining the mechanisms that generate population structure is essential to the understanding of speciation and the evolution of biodiversity. Here, we investigate a geographical range that transects two habitat gradients, the North Sea to North Atlantic transition, and the temperate to subpolar regions. We studied the harbour porpoise (Phocoena phocoena), a small odontocete inhabiting both subpolar and temperate waters. To assess differentiation among putative populations, we measured morphological variation at cranial traits (N = 462 individuals) and variation at eight microsatellite loci for 338 of the same individuals from Norwegian, British and Danish waters. Significant morphological differentiation reflected the size of the buccal cavity. Porpoises forage in relatively shallow waters preying mainly on benthic species in British and Danish waters, and on mesopelagic and pelagic fish off the coast of Norway. We suggest that the observed differentiation may be explained by resource specialization and either adaptation or developmental responses to different local habitats.     

Effects of temperature acclimation on body mass and energy budget in the Chinese bulbul Pycnonotus sinensis

Chinese bulbuls(Pycnonotus sinensis) are small passerine birds that inhabit areas of central, southern and eastern China. Previous observations suggest that free–living individuals of this species may change their food intake in response to seasonal changes in ambient temperature. In the present study, we randomly assigned Chinese bulbuls to either a 30 °C or 10 °C group, and measured their body mass(BM), body temperature, gross energy intake(GEI), digestible energy intake(DEI), and the length and mass of their digestive tracts over 28 days of acclimation at these temperatures. As predicted, birds in the 30 °C group had lower body mass, GEI and DEI relative to those in the 10 °C group. The length and mass of the digestive tract was also lower in the 30 °C group and trends in these parameters were positively correlated with BM, GEI and DEI. These results suggest that Chinese bulbuls reduced their absolute energy demands at relatively high temperatures by decreasing their body mass, GEI and DEI, and digestive tract size.