Digestive Flexibility Research Articles

Composition and Adaptation of the Enteric Neural System in Laboratory Rodents: A Cellular Overview

The enteric nervous system (ENS) is a neuron network present in the digestive system. Intestinal tract anatomic differences and cellular composition in different animals can help with interaction with environmental comprehension, which is a pertinent theme in molecular and cellular neurophysiology. In mammals, ENS is not the same in all species; rodents, generally, are great models for digestive tract adaptation study in physiologic process and environmental adaptation interpretation. This study is a narrative overview that describes morphological and cellular composition characterization in rodent neural enteric systems. Interstitial Cajal cells structural characteristics; ENS embryonic cell; system adaptation mediated by fasting, acute and chronic starve; gestation and lactation; temperature and diet; parasitism and rodent caloric restriction were aborded. Seasonal or transitory changes in intestine size probably occur when connected to food quality than its availability. Changes in female intestine size are reversible and periodic, increasing during lactation rodent as an attractive model for digestive flexibility study in the intestine size adjustment area. Enteric nervous system neuron morphological classification is presented, according to digestive tract localization and animal species. In conclusion, a significant change in intestinal mass and length in different rodent species can implicate intestinal motility during and after intestinal tract injury.

The Effect of Water Temperature on Antioxidant and Digestive Flexibility in Miiuy croaker, Miichthys miiuy

Miichthys miiuy is a marine fish with high commercial value that is extensively cultured in China. Seawater temperature is an important factor that affects the cultivation of this fish. However, whether and how seawater temperature affects enzymatic activity during cultivation remains unclear. We treated M. miiuy with average body weight of 232.59 ± 48.79 g with four seawater temperature treatments (13.0, 20.0, 24.0, and 30.0 °C) for 12 days, and measured activities of liver antioxidant enzymes (SOD and CAT) and intestine digestive enzyme (lipases, amylase, and trypsin) at the beginning and end of the treatment. Temperature had a significant effect on the activity levels of antioxidant enzymes. SOD activity decreased from 13.0°C to 24.0°C, and increased at 30.0°C, where SOD activity was highest in samples placed in 30.0°C seawater, and lowest at 24.0°C. There were no clear trends in the CAT activity pattern with increasing temperature, and highest CAT activity levels were observed at 20.0°C and lowest levels were observed at 24.0°C. The activity rates of digestive enzymes were also significantly affected by temperature. However, there were no clear trends in activity pattern with increasing temperature, similar to CAT. Lipase activity was highest at 24.0°C, and amylase activity was highest at 24.0°C. Trypsin activity was similar across the different temperature treatments after 12 days of culturing. The present study investigated the effects of seawater temperature over time on the activities of antioxidant and digestive enzymes in M. miiuy, and the results will help develop better culture practices for M. miiuy.

The effect of fasting on nutritional status, organs size and isotopic composition in a Neotropical fish species (Jenynsia multidentata)

Digestive flexibility is considered an adaptive response that allows individuals to minimise maintenance costs during periods of food scarcity. Here, we evaluated changes in body condition and digestive (and energy storage) organs size during short-term (7 days) fasting in Jenynsia multidentata. Also, we analysed changes in the isotopic composition and C:N ratio (a proxy of lipids content) in the intestine, liver and muscle. Fasted animals were compared against two feeding groups: field animals and animals fed ad libitum in the laboratory. We found that intestinal length was larger in feeding and field animals than in fasting fish, while intestine and liver masses were heavier in feeding animals, followed by field animals and then by fasting individuals. Liver and intestine δ15N was higher in fasting fish than in field animals, but δ13C did not differ between both groups. Finally, body condition, C:N ratios and perivisceral fat mass, were greater in feeding and field individuals than in fasting animals. This way, our results indicate that (i) changes in digestive and energy storage organs size during fasting in fish are ubiquitous and noticeable, and (ii) nutritional status of animals should be taken in account for a proper interpretation of stable isotope results, particularly for splanchnic tissues (such as intestine and liver).

Slow Lorises (Nycticebus spp.) Really Are Slow: a Study of Food Passage Rates

The characteristics of food ingested by a primate affect its assimilation of energy by modulating food passage rate. In general, digestive time increases in folivorous primates and decreases in frugivorous primates when they are fed higher fiber diets but this relationship is understudied in exudativorous primates. We compared the food passage rate of five slow loris species. We studied 34 wild-caught slow lorises (15 Nycticebus coucang, 15 N. javanicus, and 4 N. menegensis) in an Indonesian rescue center and four captive-born slow lorises (2 N. bengalensis and 2 N. pygmaeus) in a UK institution. We fed the Indonesian subjects two different diets: a captive-type diet comprising fruits, vegetables, and insects and a wild-type diet formulated to be similar in nutrients to that consumed by slow lorises in the wild, consisting of gum, insects, vegetables, and nectar. We fed the UK subjects a diet of gum, vegetables, insects, and hard-boiled eggs. We formulated this diet to mimic the wild diet, with notably higher fiber fractions and lower soluble sugars than the previous diet. We measured two variables: the transit time (TT) and the mean retention time (MRT). We mixed 1 tsp. of glitter in bananas or gum as our markers and fed them to the slow lorises immediately before their main diet. We noted the date and time of feeding and of appearances of the marker in feces. We weighed food given and left over for each individual to calculate ingested foods and nutrients. We found that TTs were not affected by diet treatment but MRTs were significantly longer for all species fed the wild-type diet. Our results show that Nycticebus spp. have long MRTs for their body weight, and N. pygmdaeus may have the slowest MRT of all primates in relation to body mass. The digestive flexibility of exudativorous primates should allow them to maximize fermentation opportunities when they ingest more (appropriate) fiber by increasing the amount of time the fiber substrate stays in the large intestine. Exudativorous primates appear to have plastic digestive strategies that may be an adaptation to cope with relatively nutrient-poor staple food sources such as gum. The provision of gum in a captive setting may therefore provide benefits for gut health in slow lorises.

Digestive flexibility in a euryhaline crab from a SW Atlantic coastal lagoon: alkaline phosphatase activity sensitive to salinity in the hepatopancreas

We studied biochemical characteristics and the response to low salinity at short and long-term after feeding of alkaline phosphatase (AP) activity in hepatopancreas of the osmoregulator crabNeohelice granulatafrom Mar Chiquita coastal lagoon (Buenos Aires Province, Argentina) (37°32′–37°45′S 57°19′–57°26′W). The hepatopancreas exhibited a levamisole-insensitive and a levamisole-sensitive AP activity with distinct characteristics. Levamisole-insensitive activity was similar within the range of pH 7.4–9.0 and exhibited a Michaelis–Menten kinetics. Levamisole-sensitive AP activity appeared to be maximal at pH 8.5 and appeared to exhibit an allosteric kinetics. In crabs acclimated to 10 psu (hyper-regulation conditions) levamisole-insensitive and levamisole-sensitive AP activity increased (about 16-fold) over time from short term (2–4 h) to long term (120 h) after feeding while no changes occurred in crabs acclimated to 35 psu (osmoconforming conditions). The changes of AP activity along with the higher values at 120 h after feeding in 10 psu compared with those in 35 psu, and the concomitant changes in proteolytic activity, suggest a role of AP in digestive and metabolic adjustments at the biochemical level upon hyper-regulatory conditions.

Digestive flexibility in response to environmental salinity and temperature in the non-symbiotic sea anemone Bunodosoma zamponii

In spite of their ecological importance in tidal pools, studies on digestive flexibility in non-symbiotic anemones (i.e., without symbiosis throughout their life) upon changes in key environmental factors are lacking. This study constitutes the first work to investigate the response of digestive enzymes in relation to high environmental salinity and temperature in a non-symbiotic sea anemone. We determined the occurrence and biochemical characteristics of maltase activity and compared maltase and proteolytic activities in mesenterial filaments in Bunodosoma zamponii from the intertidal area of Punta Cantera, Mar del Plata, Argentina (38°05′S, 57°32′W) acclimated to 35 and 40 psu and after an acute enhancement (15 min) of temperature from 20° to 30°C. Maltase activity was higher in 40 psu and upon the increase in temperature (about 80 and 99%, respectively). Proteolytic activity was not affected in any case. The results suggest the occurrence of specific digestive adjustments in relation to high salinity and temperature. The fact that differential modulation of maltase activity could be associated with a higher digestive capacity for glycogenic substrates is discussed.

Host plant-specific remodeling of midgut physiology in the generalist insect herbivore Trichoplusia ni

Species diversity in terrestrial ecosystems is influenced by plant defense compounds that alter the behavior, physiology, and host preference of insect herbivores. Although it is established that insects evolved the ability to detoxify specific allelochemicals, the mechanisms by which polyphagous insects cope with toxic compounds in diverse host plants are not well understood. Here, we used defended and non-defended plant genotypes to study how variation in chemical defense affects midgut responses of the lepidopteran herbivore Trichoplusia ni, which is a pest of a wide variety of native and cultivated plants. The genome-wide midgut transcriptional response of T. ni larvae to glucosinolate-based defenses in the crucifer Arabidopsis thaliana was characterized by strong induction of genes encoding Phase I and II detoxification enzymes. In contrast, the response of T. ni to proteinase inhibitors and other jasmonate-regulated defenses in tomato (Solanum lycopersicum) was dominated by changes in the expression of digestive enzymes and, strikingly, concomitant repression of transcripts encoding detoxification enzymes. Unbiased proteomic analyses of T. ni feces demonstrated that tomato defenses remodel the complement of T.ni digestive enzymes, which was associated with increased amounts of serine proteases and decreased lipase protein abundance upon encountering tomato defense chemistry. These collective results indicate that T. ni adjusts its gut physiology to the presence of host plant-specific chemical defenses, and further suggest that plants may exploit this digestive flexibility as a defensive strategy to suppress the production of enzymes that detoxify allelochemicals.

Are the Most Plastic Species the Most Abundant Ones? An Assessment Using a Fish Assemblage

Few studies have evaluated phenotypic plasticity at the community level, considering, for example, plastic responses in an entire species assemblage. In addition, none of these studies have addressed the relationship between phenotypic plasticity and community structure. Within this context, here we assessed the magnitude of seasonal changes in digestive traits (seasonal flexibility), and of changes during short-term fasting (flexibility during fasting), occurring in an entire fish assemblage, comprising ten species, four trophic levels, and a 37-fold range in body mass. In addition, we analyzed the relationship between estimates of digestive flexibility and three basic assemblage structure attributes, i.e., species trophic position, body size, and relative abundance. We found that: (1) Seasonal digestive flexibility was not related with species trophic position or with body size; (2) Digestive flexibility during fasting tended to be inversely correlated with body size, as expected from scaling relationships; (3) Digestive flexibility, both seasonal and during fasting, was positively correlated with species relative abundance. In conclusion, the present study identified two trends in digestive flexibility in relation to assemblage structure, which represents an encouraging departure point in the search of general patterns in phenotypic plasticity at the local community scale.

Phenotype flexibility in wild fish: Dolly Varden regulate assimilative capacity to capitalize on annual pulsed subsidies

1. Large digestive organs increase rates of energy gain when food is plentiful but are costly to maintain and increase rates of energy loss when food is scarce. The physiological adaptations to this trade-off differ depending on the scale and predictability of variation in food abundance. 2. Currently, there is little understanding of how animals balance trade-offs between the cost and capacity of the digestive system in response to resource pulses: rare, ephemeral periods of resource superabundance. We investigated the physiological and behavioural tactics of the fish Dolly Varden (Salvelinus malma) that rear in watersheds with low in situ productivity, but experience annual resource pulses from the spawning migrations of Pacific salmon. The eggs of Pacific salmon provide high-energy food for Dolly Varden. 3. Dolly Varden sampled 6 weeks prior to the resource pulse exhibited atrophy of the stomach, pyloric caeca, intestine and liver. Throughout the portion of the growing season prior to the resource pulse, fish exhibited empty stomachs, low indices of energy condition and muscle isotope signatures reflecting the previous resource pulse. 4. During the resource pulse, Dolly Varden exhibited large digestive machinery, gorged on salmon eggs and rapidly stored energy in fat reserves, somatic growth and gonad development. Dolly Varden appeared to achieve nearly their entire annual energy surplus during the ∼ 5-week period when sockeye salmon spawn. 5. Digestive flexibility provides Dolly Varden the energy efficiency required to survive and reproduce when resource abundance is concentrated into an annual pulse that is predictable, yet highly ephemeral. Although fish are known to incur extremely variable energy budgets, our study is one of the first to document digestive flexibility in wild fish. Our study emphasizes that fish can rely heavily on rare, high-magnitude foraging opportunities. Human actions that attenuate spikes in food abundance may have stronger than anticipated effects on consumer energy budgets.

Western Purple-faced Langurs (Semnopithecus vetulus nestor) Feed on Ripe and Ripening Fruits in Human-modified Environments in Sri Lanka

Although most colobines feed mainly on leaves and a few feed heavily on seeds, colobine digestive adaptations for folivory are thought to preclude the high use of ripe fleshy fruits. In this long-term study of Semnopithecus vetulus nestor, the endemic western purple-faced langur of Sri Lanka, I investigated the feeding ecology and dietary flexibility for fruit feeding in 2 free-ranging groups (PT1 and R1) living in human-modified environments with abundant cultivated fruit, at Panadura and Piliyandala, for 19 mo and 13 mo respectively, using scan-sampling, vegetation enumeration, and phenological studies. In contrast to folivorous forest-living colobines, including other subspecies of Semnopithecus vetulus, my focal groups used more fruit (>50%) than foliage (PT1: 36%; R1: 34%). Both groups used many plant species (PT1 115; R1 59), but selected their food species, fruits over leaves, and young leaves over mature leaves. Fruit use was independent of young leaf availability. Notably, 78.4% and 83.4% of fruits consumed by PT1 and R1 were fleshy and human-edible, most of which were ripening or ripe (PT1: 72.4%; R1: 94.8%). The main fruit for both groups was Artocarpus heterophyllus (Moraceae; jakfruit), a cultivar with fleshy fruit. These findings differ from previous understanding of colobine diets. I suggest that environmental factors, such as the abundance and nature of available fruits, and the absence of arboreal-primate fruit competitors, could influence the use of ripe fleshy fruits by colobines strongly, highlighting the need to review the dietary and digestive flexibility of this group in changed and changing natural environments to formulate effective conservation action.

Digestive flexibility during fasting in the characid fishHyphessobrycon luetkenii

Digestive flexibility is a widespread phenomenon among animals, and the congruence between empirical data and optimal digestion models strongly supports the idea that it has evolved by natural selection. However, current understanding of the evolution of this amazing flexibility is far from being comprehensive. Evidence from vertebrate tetrapods suggests that there are two major mechanisms for intestinal down-regulation during fasting periods: a decrease in the number of enterocytes in the mucosal epithelium in endothermic species, and a transitional epithelium in concert with a marked hypotrophy of enterocytes in ectothermic species. Here, we analyze the intestinal changes, at the morphological and histological levels, occurring after 9 and 16 days of fasting in a small characid fish species (Hyphessobrycon luetkenii). We found that short-term fasting was correlated with a marked down-regulation of gut size (i.e., caeca and intestine dry mass fall to a 42.3%, while intestinal length was reduced to a 73.9% of the feeding values) and that these changes were accompanied by a shift in intestinal epithelial organization from a simple columnar to pseudostratified one. This result, in conjunction with data on changes in enterocyte turnover rates during fasting in other fish species, suggests that gut regulation at both levels, cell renewal rate and epithelia configuration, is the basal condition to all tetrapods. More data, especially in some key taxonomic groups (e.g., fish that follow an endothermic strategy), will be needed in order to reach a clear understanding of digestive flexibility evolution.

Fully reversible phenotypic plasticity of digestive physiology in young house sparrows: lack of long-term effect of early diet composition

Feeding conditions during the nestling period may significantly affect whole-life fitness in altricial birds but little is known about the physiological mechanisms responsible for these effects. Permanent changes (irreversible developmental plasticity) in digestive physiology caused by the neonatal diet may form such a mechanism. We previously showed that the lack of starch in the diet of house sparrow (Passer domesticus) nestlings between 3 and 12 days post-hatching significantly decreased the activity of intestinal maltase, an enzyme essential for starch digestion. To check whether diet-induced variation in maltase activity in young house sparrows is reversible, we raised them under laboratory conditions from 3 until 30 days of age on diets with either 0% starch or 25% starch, with some individuals experiencing a switch in their assigned diet at 12 days of age. We found evidence for the presence of an internal, presumably genetic, program for changes in the activity of maltase and sucrase, which was, however, significantly affected by diet composition (i.e. environmental factor). Digestive enzyme activity in 30 day old birds was not influenced by diet composition prior to day 12 but instead depended only on diet that was fed between days 12 and 30. We conclude that plasticity in the activity of intestinal disaccharidases in house sparrow nestlings represents completely reversible phenotypic flexibility that can help young sparrows to cope with unpredictable variation in food composition during ontogeny without long-term effects on their digestive system. However, comparison with other species suggests that the magnitude of digestive flexibility in young passerines may be evolutionarily matched to species-specific variation in feeding conditions.

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.

Digestive flexibility in females of the subterranean rodent ctenomys talarum in their natural habitat

We studied the occurrence of digestive strategies at different levels in females of the subterranean herbivorous rodent Ctenomys talarum living in their natural habitat. We determined the dimensions of different parts of the gastrointestinal tract and organs along as the activity of key digestive enzymes(sucrase, maltase and N-aminopeptidase) in small intestine in females seasonally caught. Females of C. talarum did not show seasonal variations in the mass of the different parts of the gastrointestinal tract. In nonreproductive females large intestine was longer in autumn, whereas reproductive females did not show seasonal variations in the length of the different parts of the gut. Females of C. talarum exhibited a high sucrose, maltase and N-aminopeptidase activity in small intestine, although these activities were higher in small intestine of females caught in autumn (nonreproductive) than in females caught in winter (reproductive). The results show that C. talarum females exhibit characteristics in the gut at the morphological and biochemical level, which could represent digestive strategies to face the constraints imposed by their costly particular way of life.

Between-population differences in digestive flexibility in the olivaceous field mouse

The flexibility of digestive traits characterizes a standard model of physiological flexibility, demonstrating that animals adjust their digestive attributes in order to maximize overall energy return. Using an intraspecific experimental study, we evaluated the amount of flexibility in digestive tract mass and length in individuals from field mouse populations inhabiting semi-arid and temperate rain forest habitats and acclimated for six months to diets of different qualities. In accordance with the predictions of the theory of digestion, we observed a highly significant relationship between dietary variability and digestive flexibility in both specific digestive chambers and in the total digestive tract mass and length. Specifically, we found higher digestive plasticity in response to diet quality in rodents inhabiting southern temperate ecosystems with higher dietary variability in comparison to individuals from northern semi-arid habitats.

Low plasticity in digestive physiology constrains feeding ecology in diet specialist, zebra finch (Taeniopygia guttata)

It can be hypothesized that species with a wide or variable food niche are able to adjust their digestive physiology to current food type. In diet specialists, however, the capacity for such presumably costly plasticity is not necessary and flexibility of digestive physiology should be lower. Recently, we found that ontogenetic changes in the activity of digestive enzymes in house sparrow, a species that gradually consumes more carbohydrates during ontogeny, are strongly modified by diet composition. In the present study we examined digestive flexibility of nestling and adult zebra finches, typical diet specialists that consume only seeds after hatching. Both adult and nestling zebra finches could not thrive on a protein-rich and carbohydrate-free diet that supported normal development of young house sparrows. Mass-specific activity of intestinal carbohydrases (maltase and sucrase) was not elevated by higher diet carbohydrate content in both nestling and adult birds. Mass-specific activity of maltase changed less during ontogenetic development in zebra finch than in house sparrow. We conclude that the digestive physiology of zebra finch is adapted to process carbohydrate-rich food after hatching and is much less flexible than in house sparrow. We hypothesize that this difference might reflect the lack of a diet switch during ontogeny or result from high specialization to a narrow diet niche.

Consumption and digestion of animal food by rocky intertidal herbivores: an evaluation of digestive flexibility and omnivory in three grazing species

The ingestion of invertebrates by herbivores on rocky intertidal shores is traditionally considered a casual phenomenon. However, a recent study of 29 species in northern Chile shows that animal consumption is widespread, consistent, and important, suggesting that some of these herbivores may actually be omnivores. Therefore, we examined the capability of three common Chilean herbivores (the key-hole limpets Fissurella limbata and Fissurella picta and the polyplacophoran Chiton granosus ) to digest animal food. For each species, we conducted no-choice feeding experiments using artificial foods based on either algal or animal tissue from one of their frequent prey ( Ulva rigida , Perumytilus purpuratus ). After the feeding trials, we evaluated the total proteolytic activity (availability of free amino acids) in the digestive contents of the species studied and, as a reference, we evaluated this activity in animals obtained directly from the field. We found that all three species were able to eat animal food, and this consumption was not significantly different from that of algal food, suggesting that both foods were not only edible but at least similarly palatable. In addition, we detected comparable levels of proteolytic activity under the three feeding conditions for the three species. No statistical differences were found for C. granosus , but activity was significantly higher with animal food in F. limbata and with algal food in F. picta . Our data show the high digestive flexibility of these species, suggesting their ability for adaptive modulation and the possibility that they are true omnivorous consumers. We discuss the implications of these results for our current view of the structure of rocky intertidal food webs.

Consumption and digestion of animal food by rocky intertidal herbivores: an evaluation of digestive flexibility and omnivory in three grazing species.

Consumption and digestion of animal food by rocky intertidal herbivores: an evaluation of digestive flexibility and omnivory in three grazing species.

Gut Size Variation AmongBufo spinulosusPopulations Along an Altitudinal (and Dietary) Gradient

To date, digestive flexibility has been studied in dozens of vertebrate species. However, practically all of these works has ignored the importance of intraspecific physiological variability across populations inhabiting different habitats. Here, we compare the digestive tract gross morphology of three populations of the Andean toad (Bufo spinulosus), inhabiting along an altitudinal gradient and feeding on different food items. Results support a core prediction of digestive theory, i.e., intestinal length increases in parallel with the content of indigestible material in the natural diet. The present study suggest how variation in the abiotic environment associated with altitude (e.g., temperature, water availability, soil quality) can change biotic conditions (e.g., vegetation cover, prey availability), affect feeding behavior of individuals (e.g., width and composition of trophic niche), and, ultimately, individuals' digestive features (e.g., gut morphology).

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.