Paweł Brzęk

Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition.

SUMMARY House sparrow nestlings are fed primarily on insects during the first 3 days of their life, and seeds become gradually more important afterwards. We tested whether developmental changes in size and functional capacity of the digestive tract in young house sparrows are genetically hard-wired and independent of diet, or can be modified by food type. Under laboratory conditions, we hand-fed young house sparrows with either a starch-free insect-like diet, based mainly on protein and fat, or a starch-containing diet with a mix of substrates similar to that offered to older nestlings in natural nests when they are gradually weaned from an insect to a seed diet. Patterns of overall development in body size and thermoregulatory ability, and in alimentary organ size increase, were relatively similar in house sparrow nestlings developing on both diets. However, total intestinal maltase activity, important in carbohydrate breakdown, was at least twice as high in house sparrow nestlings fed the starch-containing diet (P<0.001). The change in maltase activity of nestlings was specific, as no change occurred in aminopeptidase-N activity in the same tissues. There was no significant diet effect on digesta retention time, but assimilation efficiency for radiolabeled starch tended to be higher (P=0.054) in nestlings raised on starch-containing diet. Future studies must test whether the diet-dependent increase in maltase activity during development is irreversible or reversible, reflecting, respectively, a developmental plasticity or a phenotypic flexibility.

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

SUMMARY 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.

Pancreatic and intestinal carbohydrases are matched to dietary starch level in wild passerine birds.

Evolutionary shifts in diet composition are presumably accompanied by simultaneous changes in digestive physiology. The adaptive modulation hypothesis predicts that activities of digestive enzymes should match the relative levels of their substrates in an animal’s diet so that available membrane space and synthetic energy are not wasted on enzymes in excess of need. However, previous studies on captive passerine birds showed high intraspecific phenotypic flexibility only in proteases but not in carbohydrases in response to varying diet composition. In this study, we measured the activities of pancreatic, intestinal, and hepatic enzymes in six wild-caught passerine species. We predicted that if the adaptive modulation hypothesis holds during evolutionary shifts in diet composition in birds, then mass-specific activities of digestive enzymes should be correlated positively with the content of their relevant substrates in species’ diets. Whereas mass-specific activities of proteases (aminopeptidase-N, trypsin, chymotrypsin, alanine aminotransferase) were not correlated with estimated dietary protein content, mass-specific activities of all studied carbohydrases (amylase, maltase, sucrase) were positively correlated with estimated dietary starch content. We conclude that activities of carbohydrases but not proteases are evolutionarily matched to diet composition in passerine birds. We hypothesize that the need for nitrogen and essential amino acids can prevent the evolution of a low activity of proteases, even in species feeding on a low-protein diet.

High basal metabolic rate does not elevate oxidative stress during reproduction in laboratory mice

Increased oxidative stress (OS) has been suggested as a physiological cost of reproduction. However, previous studies reported ambiguous results, with some even showing a reduction of oxidative damage during reproduction. We tested whether the link between reproduction and OS is mediated by basal metabolic rate (BMR), which has been hypothesized to affect both the rate of radical oxygen species production and antioxidative capacity. We studied the effect of reproduction on OS in females of laboratory mice divergently selected for high (H-BMR) and low (L-BMR) BMR, previously shown to differ with respect to parental investment. Non-reproducing L-BMR females showed higher oxidative damage to lipids (quantified as the level of malondialdehyde in internal organ tissues) and DNA (quantified as the level of 8-oxodG in blood serum) than H-BMR females. Reproduction did not affect oxidative damage to lipids in either line; however, it reduced damage to DNA in L-BMR females. Reproduction increased catalase activity in liver (significantly stronger in L-BMR females) and decreased it in kidneys. We conclude that the effect of reproduction on OS depends on the initial variation in BMR and varies between studied internal organs and markers of OS.

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

SUMMARY 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.

Effect of dietary restriction on metabolic, anatomic and molecular traits in mice depends on the initial level of basal metabolic rate

SUMMARY Dietary restriction (DR)-related delay of ageing is hypothesized to be mediated by the reduction of the metabolic rate (MR). However, studies on the effect of DR on MR have produced equivocal results. We demonstrated that this lack of congruency can be due to a variation in the initial level of MR within a given pool of experimental subjects. We subjected laboratory mice from two line types divergently selected for basal MR (BMR) to 30% DR lasting 6 months to test whether the effect of DR depends on the initial variation in BMR and peak MR. BMR and peak MR were independently affected by DR. The effect of DR was stronger in line types with higher initial levels of MR. Line-type-specific changes in the proportions of body components explained contrasting effects of DR on the mass-corrected BMR, which decreased in the high-BMR line type and did not change in the low-BMR line type. We conclude that the initial variation in MR can significantly affect response to DR. However, we found no association between the level of MR and mechanisms underlying the susceptibility to or protection against oxidative stress.

Effect of age and diet composition on activity of pancreatic enzymes in birds

Digestive enzymes produced by the pancreas and intestinal epithelium cooperate closely during food hydrolysis. Therefore, activities of pancreatic and intestinal enzymes processing the same substrate can be hypothesized to change together in unison, as well as to be adjusted to the concentration of their substrate in the diet. However, our knowledge of ontogenetic and diet-related changes in the digestive enzymes of birds is limited mainly to intestinal enzymes; it is largely unknown whether they are accompanied by changes in activities of enzymes produced by the pancreas. Here, we analyzed age- and diet-related changes in activities of pancreatic enzymes in five passerine and galloanserine species, and compared them with simultaneous changes in activities of intestinal enzymes. Mass-specific activity of pancreatic amylase increased with age in young house sparrows but not in zebra finches, in agreement with changes in typical dietary starch content and activity of intestinal maltase. However, we found little evidence for the presence of adaptive, diet-related modulation of pancreatic enzymes in both passerine and galloanserine species, even though in several cases the same birds adaptively modulated activities of their intestinal enzymes. In general, diet-related changes in mass-specific activities of pancreatic and intestinal enzymes were not correlated. We conclude that activity of pancreatic enzymes in birds is under strong genetic control, which enables evolutionary adjustment to typical diet composition but is less adept for short term, diet-related flexibility.

Activity of intestinal carbohydrases responds to multiple dietary signals in nestling house sparrows

SUMMARY The ‘adaptive modulation hypothesis’ predicts that activity of digestive enzymes should match the amount of their substrates in diet. Interestingly, many passerine birds do not adjust the activity of intestinal carbohydrases to dietary carbohydrate content. It is difficult to assess the generality of this rule, because in some studies passerines fed on low-carbohydrate and high-lipid diet showed reduced activity of intestinal carbohydrases. However, as carbohydrase activity may be inhibited by high dietary lipid content, it is unclear whether observed effects reflected lack of induction by the low carbohydrate levels or suppression by the high lipid levels. Here, we isolated the specific effects of dietary carbohydrate and lipid on carbohydrases. We hand-fed house sparrow nestlings on diets with 25% starch and 8% lipid (diet HS), no starch and 20% lipid (HL), or 25% starch and 20% lipid (HSL). Our results show that activity of intestinal carbohydrases is simultaneously induced by dietary carbohydrates and decreased by dietary lipid, although the latter effect seems stronger. Activities of maltase and sucrase summed over the total intestine decreased in the order HS>HSL>HL. We observed a complex interaction between diet composition and intestinal position for mass-specific activity of these enzymes, suggesting site-specific responses to changes in digesta composition along the intestines caused by digestion and absorption. We re-interpret results of earlier studies and conclude that there is no unequivocal example of adaptive modulation of intestinal carbohydrases by dietary carbohydrate in adult passerine birds, whereas the present experiment confirms that nestlings of at least some species possess such capacity.

Effect of Age and Diet on Total and Paracellular Glucose Absorption in Nestling House Sparrows

Size and hydrolytic activity of the gastrointestinal tracts of altricial birds undergo large and rapid changes during ontogeny. However, nothing is known about the development of the capacity of absorption of products of digestion, a factor that can limit total digestive performance. Using pharmacokinetic methods applied to wild‐collected and laboratory‐raised altricial nestlings of house sparrows (Passer domesticus), we addressed several questions of general significance about absorption in young birds. We found that both rate and efficiency of absorption of radiolabeled 3‐O‐methyl‐d‐glucose (3‐OMD‐glucose; absorbed by both transporter‐mediated and nonmediated mechanisms) increased significantly between days 3 and 12 posthatch. We hypothesize that these changes can explain improvements in whole‐diet digestion rate and efficiency observed in the young of house sparrows and of many other avian species, even after intestinal growth has ceased. We also tested the hypothesis that a high level of nonmediated, paracellular glucose absorption, as is typical in adult house sparrows, would already be observed in nestlings, and that their glucose absorption efficiency would not depend on glucose load because absorption rate is nonsaturable and is matched to substrate concentration. Using l‐glucose (which is absorbed by nonmediated mechanism[s]), we found that, as predicted, paracellular absorption accounted for the majority of total absorption in nestlings of all ages, and starch content (0% vs. 25%) in the diet of laboratory‐raised nestlings had no effect on efficiency of absorption of 3‐OMD‐glucose. Presumably, reliance on nonmediated absorption in young sparrows can save energy for growth. Also, during the transition from an almost starch‐free, insect‐based diet during the first days posthatch to the starch‐rich, seed‐based diet that is typical of adults, reliance on passive absorption is advantageous because the rate of absorption can easily match the current carbohydrate level in the intestines and the activity of hydrolytic enzymes.

Differential transcriptional responses underlie dietary induction of intestinal carbohydrase activities in house sparrow nestlings

Many species show diet-induced flexibility of activity of intestinal enzymes; however, molecular and genetic mechanisms responsible for such modulation are less known, particularly in altricial birds. The goal of our study was to test whether a diet-induced increase in activity of intestinal maltase and sucrase in house sparrow nestlings is matched with an increase in maltase-glucoamylase (MG) and sucrase-isomaltase (SI) complex mRNAs respectively. Both enzyme activities were significantly higher in mid-intestine of nestlings fed a medium-starch (MS) diet compared to those fed a starch-free (SF) diet. In contrast to the similar pattern of dietary induction for both enzyme activities, diet MS elevated significantly only the level of MG mRNA, but not SI mRNA. The coordinated increase in activity of maltase and in MG mRNA is consistent with the hypothesis that dietary induction of this enzyme is under transcriptional control. In contrast, the lack of such coordination for changes in activity of sucrase and SI mRNA suggests that upregulation of this enzyme may be achieved by post-translational factor(s). We conclude that genetic mechanisms responsible for diet-induced flexibility of digestive enzymes in birds may differ from that observed in mammals.