Post-ingestive Processes Research Articles

Towards an integrated understanding of dietary phenotypes.

Diet and nutrition comprise a complex, multi-faceted interface between animal biology and food environments. With accumulating information on the many facets of this association arises a need for systems-based approaches that integrate dietary components and their links with ecology, feeding, post-ingestive processes and the functional and ecological consequences of these interactions. We briefly show how a modelling approach, nutritional geometry, has used the experimental control afforded in laboratory studies to begin to unravel these links. Laboratory studies, however, have limited ability to establish whether and how the feeding and physiological mechanisms interface with realistic ecological environments. We next provide an overview of observational field studies of free-ranging primates that have examined this, producing largely correlative data suggesting that similar feeding mechanisms operate in the wild as in the laboratory. Significant challenges remain, however, in establishing causal links between feeding, resource variation and physiological processes in the wild. We end with a more detailed account of two studies of temperate primates that have capitalized on the discrete variation provided by seasonal environments to strengthen causal inference in field studies and link patterns of intake to dynamics of nutrient processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Unequal rewarding of three metabolizable sugars - sucrose, fructose and glucose - in olfactory learning and memory in Bactrocera dorsalis.

Learning and memory are the most characterized advanced neurological activities of insects, which can associate information with food. Our previous studies on Bactrocera dorsalis have shown that this fly can learn to evaluate the nutritional value of sugar rewards, although whether all metabolizable sugars are equally rewarding to flies is still unclear. To address this question, we used three sweet and metabolizable sugars - sucrose, fructose and glucose - as rewards for conditioning. The flies showed differences in learning and memory in response to the three sugar rewards. The level of learning performance in sucrose-rewarded flies was higher than that in fructose-rewarded and glucose-rewarded flies, and, strikingly, only sucrose and glucose stimulation led to the formation of robust 24-h memory. Furthermore, the unequal rewarding of three sugars was observed in two distinct processes of memory formation: preingestive and postingestive processes. When flies received the positive tastes (preingestive signal) by touching their tarsi and proboscis (mouthparts) to three sugars, they showed differences in learning for the three sugar rewards. The formation of a robust 24-h memory was dependent on the postingestive signal triggered by feeding on a sugar. A deficit of 24-h memory was observed only in fructose-feeding flies no matter what sugar was used to stimulate the tarsi. Taken together, our results suggest that three sweet and metabolizable sugars unequally rewarded B. dorsalis, which might be a strategy for flies to discriminate the nature of sugars.

Electrophoretic protein profiles of mid-sized copepod Calanoides patagoniensis steadily fed bloom-forming diatoms

Recent field and experimental evidence collected in the southern upwelling region off Concepción (36°5’S, 73°3’W) showed an abrupt reduction (<72 h) in the egg production rates (EPR) of copepods when they were fed steadily and solely with the local bloom-forming diatom Thalassiosira rotula. Because diatoms were biochemically similar to dinoflagellate Prorocentrum minimum, a diet which supported higher reproductive outcomes, the fecundity reduction observed in copepod females fed with the diatom may have obeyed to post-ingestive processes, giving rise to resources reallocation. This hypothesis was tested by comparing feeding (clearance and ingestion rates), reproduction (EPR and hatching success) and the structure of protein profiles (i.e., number and intensity of electrophoretic bands) of copepods (adults and eggs) incubated during 96 h with the two food conditions. The structure of protein profiles included molecular sizes that were calculated from the relative mobility of protein standards against the logarithm of their molecular sizes. After assessing the experimental conditions, feeding decreased over time for those females fed with T. rotula, while reproduction was higher in females fed with P. minimum. Electrophoretic profiles resulted similar mostly at a banding region of 100 to 89-kDa, while they showed partial differences around the region of 56-kDa band, especially in those females fed and eggs produced with T. rotula. Due to reproductive volume was impacted while larvae viability, a physiological processes with specific and high nutritional requirements, was independent on food type; post-ingestive processes, such as expression of stress-related proteins deviating resources to metabolic processes others than reproduction, are discussed under framework of nutritional-toxic mechanisms mediating copepod-diatoms relationships in productive upwelling areas.

Conditioned flavor preferences in animals: Merging pharmacology, brain sites and genetic variance

The elucidation of the behavioral, neurochemical, neuroanatomical and genetic substrates mediating the development of conditioned flavor preferences (CFP) is one of the multi-faceted scientific contributions that Dr. Anthony Sclafani has made to the study of food intake. This review summarizes the results of thirty-five publications over nearly twenty years of collaborations between the Sclafani and Bodnar laboratories. This includes the different approaches employed to study the orosensory (flavor-flavor) and post-ingestive (flavor-nutrient) processes underlying CFP including its acquisition (learning) and expression. It describes how CFP is elicited by different sugars (sucrose, glucose, fructose) and fats (corn oil) in rats, and how strain-specific CFP effects can be observed through the use of inbred mouse strains to evaluate genetic variance. The roles of pharmacological substrates (dopamine, glutamate, opioids, acetylcholine, GABA, cannabinoids) mediating sugar- and fat-CFP acquisition and expression are elucidated. Finally, neuroanatomical sites of action (nucleus accumbens, amygdala, medial prefrontal and orbital frontal cortices, lateral hypothalamus) are evaluated at which dopamine signaling mediates acquisition and expression of different forms of CFP.

The role of dopamine in the pursuit of nutritional value

Acquiring enough food to meet energy expenditure is fundamental for all organisms. Thus, mechanisms have evolved to allow foods with high nutritional value to be readily detected, consumed, and remembered. Although taste is often involved in these processes, there is a wealth of evidence supporting the existence of taste-independent nutrient sensing. In particular, post-ingestive mechanisms arising from the arrival of nutrients in the gut are able to drive food intake and behavioural conditioning. The physiological mechanisms underlying these effects are complex but are believed to converge on mesolimbic dopamine signalling to translate post-ingestive sensing of nutrients into reward and reinforcement value. Discerning the role of nutrition is often difficult because food stimulates sensory systems and post-ingestive pathways in concert. In this mini-review, I discuss the various methods that may be used to study post-ingestive processes in isolation including sham-feeding, non-nutritive sweeteners, post-ingestive infusions, and pharmacological and genetic methods. Using this structure, I present the evidence that dopamine is sensitive to nutritional value of certain foods and examine how this affects learning about food, the role of taste, and the implications for human obesity.

Response of a Generalist Herbivore Trichoplusia ni to Jasmonate-Mediated Induced Defense in Tomato

The up-regulation of plant defense-related toxins or metabolic enzyme binding proteins often leads to a negative effect on herbivorous insects. These negative effects can manifest themselves at three points: changes in food ingestion, post-ingestive-changes, and post-digestive changes. Many studies have related the decrease in herbivore growth and/or survival with expression of chemicals that interfere with post-digestive effects such as the anti-nutritive effects of protease inhibitors. Nevertheless, it is unclear whether such compounds impact herbivores via earlier ingestive processes. We addressed this question by using a jasmonate-deficient mutant (Def-1), a jasmonate-overexpressor mutant (Prosystemin or Prosys), and wild-type tomato in three trials with 5th instar Trichoplusia ni. Decreases in relative growth rate (RGR) confirmed that T. ni fed on the Prosys plants developed poorly compared to those feeding on Def-1 plants (larvae on wild-types were intermediate). Preingestive and postingestive processes contributed to this effect. Total food ingested and the consumptive index were 25% lower on Prosys plants compared to Def-1 plants. Post-ingestive processes, measured by approximate digestibility, were 62% greater on Prosy plants. Post-digestive efficiency measured by conversion of ingested and digested food (ECI and ECD) decreased on Prosys plants two-fold compared to Def-1 plants. This post-digestive interference correlated well with the 2-fold decrease in activity of digestive enzymes, serine proteases, in Prosys-fed T. ni compared to those on Def-1 plants. No difference in detoxifying enzyme activity was detected.

Endogenous nociceptin modulates diet preference independent of motivation and reward

Previous studies show that the opioid peptide nociceptin stimulates food intake. Here, we studied nociceptin receptor knockout (NOP KO) mice in various behavioral paradigms designed to differentiate psychological and physiological loci at which endogenous nociceptin might control feeding. When presented a choice under food restriction, NOP KO mice displayed reduced preference for high sucrose diet, but lower intake of high fat diet under no-choice conditions. These responses were absent under ad libitum feeding conditions. Conditioned place preference to high fat diet under food-deprived conditions was unaltered in NOP KO mice, suggesting no difference in reward responses. Furthermore, operant food self-administration under a variety of conditions showed no genotype-dependent differences, suggesting no differences in the motivational properties of food. Taste reactivity to sucrose was unchanged in NOP KO mice, though NOP KO mice had altered aversive reactions to quinine solutions under ad libitum feeding, suggesting minor differences in the affective impact of palatable and unpalatable tastants. Although NOP KO mice re-fed following food-deprivation showed normal increases in plasma glucose and insulin, multidimensional scaling analysis showed that the relationship between these measures, body weight and plasma leptin was substantially disrupted in NOP KO, particularly in fasted mice. Additionally, the typical positive relationship between body weight and plasma leptin was considerably weaker in NOP KO mice. Together, these findings suggest that endogenous nociceptin differentially modulates diet preference depending on macronutrient content and homeostatic state, independently of the motivating, rewarding or orosensory properties of food, but may involve metabolic or postingestive processes.

Amino acid and carbohydrate preferences in C57BL/6ByJ and 129P3/J mice

Compared with mice from the 129P3/J (129) inbred strain, mice from the C57BL/6ByJ (B6) inbred strain have higher consumption of several sweet-tasting amino acids and carbohydrates. To examine the relative contribution of taste and nutritive properties in these strain differences, we measured responses of B6 and 129 mice to eight sweet and non-sweet amino acids and carbohydrates in two-bottle preference tests with water. Mice from the two strains did not differ in consumption of non-sweet l-valine and l-histidine. Compared with 129 mice, B6 mice had higher consumption and lower preference thresholds for sweet amino acids l-glutamine, l-alanine and l-threonine, monosaccharides glucose and fructose, and maltooligosaccharide. These data suggest that differences in gustatory responsiveness are an important factor underlying higher consumption of some amino acids and carbohydrates by B6 mice compared with 129 mice. It is likely that in B6 mice, higher sweet taste responsiveness results in increased consumption of sweet-tasting amino acids and sugars, and higher taste responsiveness to complex carbohydrates results in increased consumption of maltooligosaccharide. However, postingestive processes also influence nutrient consumption and may be responsible for higher intake of carbohydrates compared with sweet-tasting amino acids. Results of this study set the stage for genetic analysis of differences between B6 and 129 mice in taste responsiveness and macronutrient consumption.

Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense

Almost half the biogenic sulfur emitted globally originates as dimethylsulfide (DMS) in marine algae. Yet, despite its importance to climate and the global sulfur cycle, the reasons why many diverse algal taxa produce DMS remain unclear. DMS is produced when dimethylsulfoniopro- pionate (DMSP) is cleaved by the enzyme DMSP lyase into DMS and acrylic acid. Because acrylic acid can deter feeding by some herbivores, the production of DMSP has been postulated to be part of an antiherbivore chemical defense system, with DMS being a by-product of the production of the defensive compound acrylic acid. However, we found that DMS plays a more direct role in herbivore deterrence. Using laboratory bioassays, we demonstrated that DMS functions as a potent feeding deterrent against sea urchins Strongylocentrotus droebachiensis at a wide range of concentrations. The defensive function of DMSP cleavage is further supported by the results of a multiple-choice feeding preference assay in which we offered urchins a choice of 8 algal species. In these assays, algae containing DMSP tended to be consumed at lower rates than species that lacked it. By measur- ing headspace DMS concentrations during grazing, we showed that DMS is produced when urchins feed on algae containing DMSP, but not when urchins feed on algae without it. DMS production occurred while the urchins were feeding on the algae and for 18 h after the algae were removed, suggesting that post-ingestive processes might be playing a role in activation. These results demon- strate that DMS is produced when urchins feed on algae containing DMSP and that it functions as an herbivore deterrent, causing species that produce DMSP to be avoided by some herbivores.

Effects of food nutrient content, insect age and stage in the feeding cycle on the FMRFamide immunoreactivity of diffuse endocrine cells in the locust gut.

We have studied the influence of variations in dietary protein and digestible carbohydrate content, of insect age and of time during the feeding cycle on the endocrine cells of the ampullar region of the midgut in the African migratory locust Locusta migratoria L. Morphometric analysis of FMRFamide-like immunoreactivity was used as an indirect measure of the amount of FMRFamide-related peptides (FaRPs) stored in the gut endocrine cells. There was a highly significant correlation between FaRP content and the nutritional quality of the food, measured relative to the concentrations and ratio of protein to digestible carbohydrate in a nutritionally optimal diet. The direction of the relationship between FaRP content and diet quality varied with age during the fifth stadium. On day 1, FaRP levels increased with the nutritional quality of the food, while on day 4 the opposite relationship was observed. Release of peptide was triggered by the onset of a meal during ad libitum feeding, with cell FaRP levels returning to premeal values within 15 min of the meal ending. The results also suggested that cell contents were released during food deprivation beyond the normal intermeal interval. Locusts switched for a single meal during ad libitum feeding on day 4 from a low- to a high-carbohydrate food did not respond by reducing endocrine cell FaRP content. Our results show a relationship between the diffuse gut endocrine system and feeding and nutrition in locusts. The ampullar endocrine cells are in three-way contact with the midgut luminal contents, with the primary urine from the Malpighian tubules and with the haemolymph. They are thus ideally positioned to play an integrative receptor-secretory function in the regulation of a variety of post-ingestive processes, such as enzyme secretion, absorption, gut motility or nutrient metabolism.