Digestive Plasticity Research Articles

Biochemical features and modulation of digestive enzymes by environmental temperature in the greater amberjack, Seriola dumerili

The study of fish digestive biochemistry is essential to understand factors that affect the net efficiency of food transformation and growth, and therefore aquaculture profitability. The aim of the present study was to assess the activity and functional characteristics of key digestive enzymes in juveniles of greater amberjack (Seriola dumerili), as well as the possible modulation of their relative importance by water temperature. For that, a combination of biochemical assays and substrate-SDS-PAGE were used. Under physiological conditions pepsin activity was negligible. Chymotrypsin was the most active enzyme in the digestive tract of the greater amberjack, while lipase was the enzyme with lower activity, though both enzymes in addition to trypsin were responsive to water temperature as revealed by discriminant analysis. Seriola dumerili showed to have pH-sensitive and, except for chymotrypsin, thermally robust proteases. Inhibition assays showed the major importance of serine proteases and revealed inverse trypsin and chymotrypsin responses to environmental temperature, with higher trypsin contribution in 26°C-fish while higher chymotrypsin contribution in 18°C-fish. Zymograms revealed three isotrypsin and three isochymotrypsin enzymes, with no variation in the presence of particular isoforms among rearing temperatures. However, they confirmed the role of chymotrypsin activity in providing digestive plasticity, with one of the isoforms being more active at lower temperatures. Thus, results indicate that variation in the relative contribution of chymotrypsin isoenzymes to a particular environmental temperature occurs due to different physic-chemical features of isoforms as a source of functional flexibility. This study assessed for the first time the effects of rearing temperature on greater amberjack digestive enzymes, increasing the knowledge on its digestive biochemistry, and aiding in the improvement of management practices for this species industrialization.

Gut Microbiome Analyses of Wild Migratory Freshwater Fish (Megalobrama terminalis) Through Geographic Isolation.

Gut microbiome is considered as a critical role in host digestion and metabolic homeostasis. Nevertheless, the lack of knowledge concerning how the host-associated gut microbiome underpins the host metabolic capability and regulates digestive functions hinders the exploration of gut microbiome variation in diverse geographic population. In the present study, we selected the black Amur bream (Megalobrama terminalis) that inhabits southern China drainage with multiple geographic populations and relatively high digestive plasticity as a candidate to explore the potential effects of genetic variation and environmental discrepancy on fish gut microbiome. Here, high-throughput 16S rRNA gene sequencing was utilized to decipher the distinct composition and diversity of the entire gut microbiota in wild M. terminalis distributed throughout southern China. The results indicated that mainland (MY and XR) populations exhibited a higher alpha diversity than that of the Hainan Island (WS) population. Moreover, a clear taxon shift influenced by water temperature, salinity (SA), and gonadosomatic index (GSI) in the course of seasonal variation was observed in the gut bacterial community. Furthermore, geographic isolation and seasonal variation significantly impacted amino acid, lipid, and carbohydrate metabolism of the fish gut microbiome. Specifically, each geographic population that displayed its own unique regulation pattern of gut microbiome was recognized as a specific digestion strategy to enhance adaptive capability in the resident environment. Consequently, this discovery suggested that long-term geographic isolation leads to variant environmental factors and genotypes, which made a synergetic effect on the diversity of the gut microbiome in wild M. terminalis. In addition, the findings provide effective information for further exploring ecological fitness countermeasures in the fish population.

Microplastics ingestion induces plasticity in digestive morphology in larvae of Xenopus laevis

Global changes in temperature, predator introductions, and pollution might challenge animals by altering food conditions. A fast-growing source of environmental pollution are microplastics. If ingested with the natural food source, microplastics act as artificial fibers that reduce food quality by decreasing nutrient and energy density with possible ramifications for growth and development. Animals might cope with altered food conditions with digestive plasticity. We examined experimentally whether larvae of the African clawed frog (Xenopus laevis) exhibit digestive morphology plasticity (i.e., gut length, mass, and diameter) in response to microplastics ingestion. As natural systems contain non-digestible particles similar in size and shape to microplastics, we included cellulose as a natural fiber control group. Gut length and mass increased in response to microplastics and cellulose ingestion indicating that both types of fibers induced digestive plasticity. Body mass and body condition were similar across experimental groups, indicating that larvae fully compensated for low nutrient and energy density by developing longer intestines. The ability of a species to respond plastically to environmental variation, as X. laevis responded, indicates that this species might have the potential to cope with new conditions during global change, although it is uncertain whether this potential may be reduced in a multi-stressor environment.

Modelling the maximal active consumption rate and its plasticity in humans-perspectives from hot dog eating competitions.

Gut capacity and plasticity have been examined across multiple species, but are not typically explored in the context of extreme human performance. Here, I estimate the theoretical maximal active consumption rate (ACR) in humans, using 39 years of historical data from the annual Nathan's Famous Hot Dog Eating Contest. Through nonlinear modelling and generalized extreme value analysis, I show that humans are theoretically capable of achieving an ACR of approximately 832 g min-1 fresh matter over 10 min duration. Modelling individual performances across 5 years reveals that maximal ACR significantly increases over time in 'elite' competitive eaters, likely owing to training effects. Extreme digestive plasticity suggests that eating competition records are quite biologically impressive, especially in the context of carnivorous species and other human athletic competitions.

Chemical composition of food induces plasticity in digestive morphology in larvae of Rana temporaria.

ABSTRACTFood conditions are changing due to anthropogenic activities and natural sources and thus, many species are exposed to new challenges. Animals might cope with altered quantitative and qualitative composition [i.e. variable protein, nitrogen (N) and energy content] of food by exhibiting trophic and digestive plasticity. We examined experimentally whether tadpoles of the common frog (Rana temporaria) exhibit phenotypic plasticity of the oral apparatus and intestinal morphology when raised on a diet of either low (i.e. Spirulina algae) or high protein, N and energy content (i.e. Daphnia pulex). Whereas intestinal morphology was highly plastic, oral morphology did not respond plastically to different chemical compositions of food. Tadpoles that were fed food with low protein and N content and low-energy density developed significantly longer guts and a larger larval stomachs than tadpoles raised on high protein, N and an energetically dense diet, and developed a different intestinal surface morphology. Body sizes of the treatment groups were similar, indicating that tadpoles fully compensated for low protein, N and energy diet by developing longer intestines. The ability of a species, R. temporaria, to respond plastically to environmental variation indicates that this species might have the potential to cope with new conditions during climate change.

Seasonal intake responses could reflect digestive plasticity in the nectar-feeding bat Anoura geoffroyi

Many studies have used intake response as a tool for understanding digestive capacities of bats to process nectar. Nevertheless, most of them have been done so in one season, assuming that this response does not change over the year. One study performed with Glossophaga soricina, a bat inhabiting warm environments, found different intake response over seasons, but these changes are unknown for other bat species; especially those inhabiting cold climates. We measured changes in volumetric intake of Anoura geoffroyi (found in places above 2, 500 m a.s.l.) feeding on sucrose concentrations ranging from 5 to 35% (wt./vol.) in spring and compared the results with those previously published for winter. Because of differences in ambient temperature and nectar availability in the places they inhabit, we predicted different intake responses among seasons. We found differences in intake responses between winter and spring. Constant energy intake in winter was 101.07 ± 5.4 kJ, and decreased from 23 to 37% in spring. Body mass gain in winter was 1.31 ± 0.1 g, and was reduced from 56 to 74% in spring, when bats fed on sugar concentrations of 15 and 5%. Seasonal differences in intake responses and body mass changes provide evidence of digestive plasticity, which may have important ecological implications for bats. Species able to change their digestive traits would have the capacity to change their food intake depending on the energy demands imposed by their environment, while those with low plasticity should change their behavioral and energy-saving strategies when confronting changes in the abundance or the nutritional quality of the nectar they consume.

Contributions of digestive plasticity to the ability of white-tailed deer to cope with a low-quality diet

Many herbivores exhibit phenotypic variations of their digestive system in response to changes in quality of food resources. This digestive plasticity is considered an adaptive trait for individuals to help them cope with variation in food resources and to fulfill nutritional needs. We investigated whether digestive phenotypic variations could contribute to sustain the population of introduced white-tailed deer ( Odocoileus virginianus ) on Anticosti Island (Quebec, Canada) facing a winter diet of low-quality forage. We compared digestive morphology and in vitro digestibility of winter forage to that of deer from the original mainland population. Deer on Anticosti Island had a higher ruminal volume and digesta load (43% and 62%, respectively), greater absorption surface of the ruminal papillae, and greater relative mass of all forestomachs than deer from the mainland. Woody forage digestibility was similar between the 2 populations, even though faster kinetic digestion may occur for deer on Anticosti Island. Digestive plasticity appears to play a central role in sustaining high deer densities facing harsh forage conditions on Anticosti Island. Comparisons of digestive morphology and digestibility between populations that have access to forage of variable quality contribute to our understanding of the digestive response and the role of digestive plasticity for individuals facing a decline in diet quality.

Post‐metamorphic carry‐over effects of larval digestive plasticity

Summary For animals with complex life cycles, conditions in the larval environment can have important effects that persist after metamorphosis. These carry‐over effects may influence juvenile growth plasticity and have important fitness consequences. Small juvenile red‐eyed treefrogs, Agalychnis callidryas, grow faster than larger ones. We examined to what extent this growth pattern is due to carry‐over effects of intraspecific larval competition. In particular, we assessed larval gut plasticity and determined whether carry‐over effects could persist given the extensive gut remodelling that occurs when herbivorous larvae transition to carnivorous juveniles. We reared larvae in mesocosms at low, medium and high densities and measured the size of both larval and juvenile guts, livers and fat bodies. We also monitored the timing of the onset of juvenile feeding post‐metamorphosis and, after the onset of feeding, we measured intake rate and mean diet retention time. Finally, we measured juvenile metabolic rates to determine whether any organ size plasticity contributed to metabolic carry‐over effects. Larval density had strong effects on larval morphology with higher densities increasing gut length and decreasing liver and fat body sizes. The effects of this plasticity carried over post‐metamorphosis. High larval densities produced smaller juveniles with proportionately longer guts and extremely small livers and fat bodies. There were no apparent carry‐over effects on size‐specific metabolic rate. Differences in larval density were also associated with differences in post‐metamorphic feeding. Small juveniles from high larval densities began feeding even before metamorphosis was complete, whereas large juveniles from low larval densities experienced a significant 2‐week delay. Although juvenile body mass varied over threefold across treatments, once feeding was initiated, neither intake nor mean diet retention time scaled with body size. Overall, high larval densities produced small juveniles with very low lipid reserves that may have stimulated hyperphagia relative to larger juveniles. Longer guts carried over from the larval stage could facilitate this by allowing small juveniles to elevate intake without sacrificing diet retention time. Patterns of intake coupled with differences in the onset of feeding explain the size‐dependent growth pattern previously reported in this and other species.

A typical browser, the roe deer, may consume substantial quantities of grasses in open landscapes

In open landscapes, grass leaves provide an abundant resource for ruminants, with potentially high nutritional value. However, their extensive digestion requires a long fermentation time, achieved through large rumen and the stratification of the rumen content. Due to anatomical and physiological differences, ruminants differ in their ability to process grass leaves. Particularly, the small roe deer, with its viscous saliva and unstratified rumen content, is generally classified as a strict browser. We hypothesised that roe deer may be able to use grass leaves in some circumstances, notably when the availability of other resources declines and when the quality of grass leaves is high. We expected that (1) grass leave consumption should be higher in open landscapes than in forest habitat because grasses are more widely available and more nutritious in open landscapes and (2) grass leave consumption should increase in winter when the availability of other resources declines. We assessed grass consumption by microscopic analysis of roe deer faecal pellets collected monthly both in forest habitat and in the surrounding open landscape. We found that both the occurrence and the proportion of grass leaves in the faeces were higher in the open landscape (predicted mean proportion 0.31) than in the forest (predicted mean proportion 0.05). In addition, the proportion of grass leaves in the faeces was higher in winter and lower in spring in both forest and open landscape. We suggest that roe deer are able to use grass leaves with unusually high nutritional quality in winter in this mild climate area. This involves a certain level of digestive plasticity to efficiently digest high quality grasses and may confer nutritional benefit to individuals feeding in an open landscape.

Digestive toxicity in grass shrimp collected along an impact gradient

Ingested pollutants may elicit digestive toxicity following incorporation into consumer tissues. This post-assimilatory toxicity may include tissue damage influencing synthesis of digestive enzymes, gut transit time and absorption of nutrients as well as pollutants by the gut epithelium. This study investigated impacts of chronic field exposure on gut residence time (GRT), feces elimination rate (FER), extracellular digestive protease activities and gut pH in grass shrimp Palaemonetes pugio. Adult shrimp were collected from differentially impacted sites within the New York/New Jersey Harbor Estuary and fed prepared meals containing fluorescent or near-infrared markers and analyzed for digestive toxicity. Relationships between digestive parameters and assimilation efficiencies (AE) for Cd, Hg and organic carbon reported previously were also analyzed. Minimum GRT did not vary significantly for field-collected shrimp, but was positively correlated with Cd, but not Hg or carbon, AE. FER was not impacted by field exposure. Digestive protease activities exhibited a marked decrease in grass shrimp from impacted field sites relative to reference shrimp. Relationships between the assimilation of elements and digestive physiology in field-collected shrimp suggest that digestive plasticity (increasing GRT) may be important in compensating for post-assimilatory digestive toxicity (reduced protease activities) in order to maintain nutrient assimilation. Stress-induced variability in digestive function among grass shrimp populations may, in turn, enhance the assimilation of non-essential elements, such as Cd.

Digestive plasticity as a response to woodland fragmentation in roe deer

AbstractDigestive plasticity, which refers to changes in digestive features due to changes in both internal and external environmental conditions, is a crucial factor for understanding the ability of species to cope with environmental changes. In Europe, agricultural intensification and the loss of forests have been major challenges for original forest dwellers, however some species, such as the European roe deer (Capreolus capreolus), have been able to successfully colonize these new habitats. In this work, we investigated the adaptation of some digestive features of roe deer to the agricultural landscapes. We assessed whether changes in local landscape structure influenced the mass of both reticulorumen (RR) and distal fermentation chamber (DFC) of 47 juvenile and adult roe deer inhabiting an agro‐ecosystem in southwest France. Woodland cover had a clear effect on diet quality (estimated by the rate of gas production of digestive contents) and DFC weight of animals. In fact, deer from the most forested landscapes showed heavier DFCs and fed on poorer quality diet (lower gas production) than their counterparts from the most open landscapes. RR mass was less influenced by the landscape openness, being the age of animals the main factor for understanding the variations of this digestive feature in our study area. We can conclude that colonizing agricultural landscapes increases the access to highly energetic and digestive resources.

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.

31.1. Digestive plasticity in birds: Mechanisms and ecological consequences

31.1. Digestive plasticity in birds: Mechanisms and ecological consequences

Digestive Plasticity in Tadpoles of the Chilean Giant Frog (Caudiverbera caudiverbera): Factorial Effects of Diet and Temperature

Anuran metamorphosis is one of the most spectacular processes in nature. Metamorphosis entails morphological transformations and extensive changes in feeding habits, such as transforming from an herbivore to a carnivore. This phenomenon is especially sensitive to environmental cues. We studied the phenotypic plasticity of intestinal morphology and enzyme activity in tadpoles of the Chilean giant frog Caudiverbera caudiverbera. We tested the effects of diet and temperature using a factorial design, which included a control of nontreated individuals. There was no significant effect of diet treatment (i.e., low- vs. high-quality diet) on any of the measured variables, including external morphology. We found significant effects of temperature on morphological traits. Temperature treatment also had significant effects on aminopeptidase-N and maltase activity. Both enzymes exhibited complex interactions with temperature along the intestine. Gut size varied significantly among temperatures, with intestines from warm-treated individuals smaller than the intestines from control and cold-treated tadpoles. Our findings suggest that phenotypic plasticity of intestinal morphology and physiology exists in larvae of this species, at least in response to temperature. However, we did not detect clear effects of diet or temperature on the timing of metamorphosis.

Digestive plasticity of the small intestine and the fermentative hindgut in a marsupial herbivore, the tammar wallaby (Macropus eugenii)

We investigated the effects of a ground, pelleted diet versus natural forage on the gross morphology of the gastrointestinal tract of a medium-sized (5–7 kg body mass) macropodid marsupial, the tammar wallaby (Macropus eugenii). The empty wet mass (g) of the small intestine of tammar wallabies maintained on a pelleted diet for 6 weeks was 22% greater than that of animals maintained on natural forage, once body mass was taken into account by ANCOVA. Similarly, the body-mass-adjusted length of the tammar wallaby caecum and proximal colon combined was 25% longer in animals maintained on the pelleted diet compared with those maintained on forage. Our data suggest that food particle size may be directly involved in controlling the size of the post-gastric alimentary tract in tammar wallabies, and thus in their diet choice and nutritional ecology. Notably, this is the first study that links phenotypic plasticity of the gut directly to diet in a marsupial and we conclude that the tammar wallaby is an excellent model for exploring the causes and consequences of digestive plasticity in macropodid marsupials.

Digestive plasticity in Mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans

Summary The consequences of plastic responses of the avian digestive tract for the potential of birds to disperse other organisms remain largely uninvestigated. To explore how a seasonal diet switch in Mallard (Anas platyrhynchos L.) influences their potential to disperse plants and invertebrates, we recorded the retention time of markers, following exposure to two diets of contrasting digestibility (trout chow vs seeds). We then recorded the retrieval and germination of Fennel Pondweed (Potamogeton pectinatus L.) seeds and Brine Shrimp (Artemia franciscana Kellogg) cysts ingested by the same birds. Gut passage rates of markers were increasingly longer in birds on the seed‐based, high‐fibre diet and shorter in birds on the animal‐based, low‐fibre one. Propagule digestibility, and thus survival to gut passage, differed between diet groups, with more seeds and fewer cysts retrieved from ducks on the animal‐based diet. Germination decreased with retention time, but was not affected by diet. Differences in passage rates of markers but not of seeds and cysts suggest no change in dispersal distances of plants and invertebrates between seasons, while differences in digestibility would affect the numbers of propagules dispersed.

Digestive plasticity and the cost of acclimation to dietary chemistry in the omnivorous leaf-eared mouse Phyllotis darwini

We examined the costs associated with acclimation in an omnivorous mouse (Phyllotis darwini) fed two contrasting diets (carbohydrate-rich and protein-rich). We studied the response of gut morphology and digestive performance in animals shifted to a novel diet at different developmental stages. When acclimated adult animals were shifted to the alternative diet, energy digestibility decreased. We also found long-term consequences to diet acclimation. Animals reacclimated for 15 days to an alternative diet did not increase digestive performance. Although no effects of diet on gut morphology were noted, a significant positive correlation between energy digestibility and small intestinal length was found, explaining most of the variability observed in energy digestibility. These results suggest that caution should be used when defining adaptive changes if the possible cost of acclimation is neglected.

Digestive plasticity of the marine benthic omnivore Nereis virens

We investigated plasticity in the digestive chemistry of the omnivorous marine benthic polychaete Nereis virens. We sought to compare the previously observed variability among species (genotypic plasticity) versus the variability within a species (phenotypic plasticity) in response to changes in diet. We found statistically significant changes in enzyme activities between worms given carnivorous versus detritivorous diets. These changes were smaller in magnitude than the among-species range, but consistent in direction. The surface tension of the gut fluid was largely unaffected by diet. However, the presence of surfactant micelles was closely linked to the presence of sediment in the diet. These results suggest that sediment ingestion induced the introduction of high concentrations of surfactants into the gut lumen, perhaps related to the adsorption of digestive agents and products onto the mineral matrix. In the context of the among-species trends found by Mayer et al. (Digestive environments of benthic macroinvertebrate guts: enzymes, surfactants and dissolved organic matter. J. Mar. Res. 1997;55(4):785–812.), Nereis virens shows greater phenotypic plasticity in its surfactant secretion than in its enzymatic response to varying food types.

Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity

The phenotypic response of digestive enzymes was assessed in two species of rodents with different foods habits. Species were Phyllotis darwini (omnivorous) and Octodon degus (herbivorous). The activity of sucrase, maltase and aminopeptidase-N were determined in vitro in animals feeding two contrasting diets. No effect of dietary chemistry on sucrase and maltase activities was observed. Nevertheless, aminopeptidase-N showed a reversible response to diet in P. darwini but not in O. degus. Through Principal Component Analysis we separated the specific and non-specific modulation of the enzymes. The analysis showed that aminopeptidase-N activity is up-regulated by dietary protein in P. darwini. Differences in the phenotypic response of this species apparently reflect the historic levels of specific substrates of the natural diets for this enzyme, linking dietary flexibility and digestive plasticity in an evolutionary context.

Dietary flexibility and intestinal plasticity in birds: a field and laboratory study.

The adaptive modulation hypothesis posits that the expression of digestive proteins should be modulated in response to intake of their respective substrates. A corollary of this hypothesis suggests that dietary flexibility and digestive plasticity should be correlated. We examined these two hypotheses in two granivorous Chilean birds (Zonotrichia capensis and Diuca diuca) that differ in dietary breadth. D. diuca is a strict granivore, whereas Z. capensis also eats insects. In field-caught birds, the activity of the intestinal dipeptidase aminopeptidase-N was positively correlated with intake of insects in Z. capensis but not in D. diuca. This is the first field documentation of modulation of intestinal enzymes by diet in birds. Intestinal maltase and sucrase activities were not correlated with seed (vs. insect) intake in either species. In the laboratory, captive birds of both species exhibited similar modulation of membrane-bound intestinal hydrolases when fed on synthetic diets of contrasting carbohydrate and protein composition. Maltase, sucrase, and aminopeptidase-N activities were significantly higher in birds fed on the carbohydrate-free than those on the carbohydrate-containing diet. Activities of the three enzymes were positively correlated. Therefore, this increase probably resulted from nonspecific increases of all enzymes resulting from intake of the carbohydrate-free diet. Principal components analysis separating the effect of diet on specific and on nonspecific modulation revealed that diet had a strong effect on nonspecific activity of intestinal enzymes in both Z. capensis and D. diuca. Diet also significantly affected aminopeptidase-N activities when the effect of diet on nonspecific modulation was removed. Birds fed on the carbohydrate-free, high-protein diet had significantly higher specific aminopeptidase-N activities than those fed on the carbohydrate-containing diet. Our results cast doubts on the notion that dietary flexibility and the plasticity of the gut's enzymes are necessarily correlated and on the general validity of the adaptive modulation hypothesis.