Daniel Afik

The Trade‐Offs Between Digestion Rate and Efficiency in Warblers and Their Ecological Implications

Frugivory in birds is associated with rapid gut passage whereas insectivory is associated with slower gut passage. This is interpreted by some avian ecologists to reflect an inherent digestive constraint on diet selection, but it could also result from dietary acclimation. We predicted that Yellow-rumped Warblers (Dendroica coronata) acclimated to fruit-, insect-, and seed-based diets would exhibit retention times that increase in that rank order, because this is the rank order of retention time across species that eat these types of food. We also predicted a trade-off between rate of processing (the inverse of retention time) and extraction efficiency. This is based on the assumption that digestive enzymes or absorptive capacity occur in the gastrointestinal tract at levels that are not in great excess, and so less contact time between enzymes and digesta reduces the extraction efficiency. To test these predictions, we measured retention time (using aqueous and lipid-phase inert markers) and extraction efficiency of glucose, sucrose, leucine, starch, and the lipid glycerol trioleate (using radio-labeled nutrients and inert markers). Our results were in accordance with predictions. Mouth-to-anus total mean retention time (TMRT) of Yellow-rumped Warblers acclimated to fruit-, insect-, and seed-based diets were, respectively, 46 ± 9, 62 ± 6, and 114 ± 9 min for polyethylene glycol (PEG, an aqueous marker) : results were similar for the lipid phase marker in most cases. But Yellow-rumped Warblers that were switched suddenly to an alternate diet did not readjust TMRT when tested 2 h later or did so incompletely. We found no diet-related morphological changes in the digestive tract, and thus attribute these results to changes in gut motility. Extraction efficiency was uniformly high across all diets for glucose (88 ± 1%), but varied among diet groups according to our prediction for leucine (range 82-94%), sucrose (58-85%), starch (9-48%), and lipid (18-82%). We review how features of the Yellow-rumped Warblers digestive system permit relatively high energy uptake across a wide variety of food types. The most notable constraining feature was a low starch hydrolysis rate, probably restricting them from relying on starchy foods. Thus, digestive strategy (i.e., a combination of retention time of food in the gut and digestive efficiency) somewhat determines diet, but in more respects diet determines strategy.

Anatomical and histological changes in the alimentary tract of migrating blackcaps (Sylvia atricapilla): a comparison among fed, fasted, food-restricted, and refed birds.

During northward migration, blackcaps that arrive to refuel at stopover sites in Israel’s Negev Desert have reduced masses of organs that are important in food digestion and assimilation. We tested several predictions from the general hypothesis that smaller organs of digestion (small intestine and pancreas) and nutrient assimilation (liver) bring about a lower capacity to consume food and that the organs must be restored before blackcaps can feed and digest at a high rate. We used a fasting protocol to create a group of blackcaps with reduced intestine and liver mass (reduced by 45% and 36%, respectively) compared with controls fed ad lib. Because most of the small intestine’s biochemical digestive capacity reside in enterocytes found on villi, we predicted and found that reduced intestinal mass in fasted blackcaps related mainly to changes in enterocytes rather than other cells and tissues such as nonabsorptive crypt cells or underlying muscle. Because migrating blackcaps that stop over to feed begin to increase in body mass only 2 d after arrival, we predicted and found a similar recovery period in blackcaps that were first fasted but then refed—the organ mass, structure, function, and ability to consume food was restored after 2 d of feeding. Another group of food‐restricted blackcaps (fed at one‐third ad lib. level) lost similar amounts of body mass as fasted blackcaps but had much greater capacity to consume food than fasted blackcaps, and so we predicted that they would exhibit little or no reduction in alimentary organs relative to controls fed ad lib. A surprising result was that, as in fasted blackcaps, in food‐restricted blackcaps, the decreases in masses of small intestine, liver, and pancreas were proportionally greater than the decreases in body mass or in masses of nonalimentary organs (heart, pectoralis). Food restriction, like fasting, caused a decrease in amount of intestinal mucosa and an alteration in the phenotype of enterocytes. These results are thus not consistent with the general hypothesis, and although they can be rationalized by assuming that blackcaps fed ad lib. have excess digestive capacity, it may also be that the physiological process or processes limiting very high feeding rate lie elsewhere than in the digestive system.

Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis

Insectivorous/frugivorous passerine species studied so far lack the ability to modulate intestinal maltase activity, in contrast to galliformes. We tested for dietary modulation of small intestine (SI) enzymes including maltase in house sparrows to understand whether the difference between the galliformes on the one hand, and the passerines on the other, reflects a phylogenetic pattern (maltase modulated in galliformes but not passerines), a dietary pattern (maltase modulated in granivores but not insectivore/frugivores), some other pattern, or chance. We also tested the prediction that intestinal peptidase activity would be increased on a high protein (HP) diet. Birds were fed three diets high in starch, protein, or lipid for 10 days. For birds on the HP diet (60.3% protein) we observed the predicted upward modulation of aminopeptidase-N activity, as compared with the lower-protein, high starch (HS) (12.8% protein) diet. In contrast, birds eating the HS diet had similar maltase and sucrase activities, and only slightly higher isomaltase activity, compared with birds eating the high protein (HP), starch-free diet. Birds eating high lipid (HL) diet had low activities of both carbohydrases and peptidase. Considering that the statistical power of our tests was adequate, we conclude that house sparrows show little or no increase in carbohydrases in response to elevated dietary carbohydrate. We cannot reject the hypothesis that maltase lability among avian species has a phylogenetic component, or that high dietary fat has a depressing effect on both carbohydrase and peptidase activities.

A Test for Passive Absorption of Glucose in Yellow-Rumped Warblers and Its Ecological Implications

In an earlier study, we found that yellow-rumped warblers had in vitro active uptake rates of D-glucose that were only a few percent of the glucose absorption rate achieved at the wholeanimal level. Here we used a pharmacokinetic technique to test whether a substantial amount of sugar can be absorbed passively. We used yellow-rumped warblers (Dendroica coronata), known for their seasonal frugivory, freely feeding on a synthetic mash formulated with naturally occurring concentrations of D-glucose. Birds absorbed 89.8% ± 1.0% (SE) of the D-glucose in the mash. When fed the same mash with trace-labeled ³H L-glucose, the stereoisomer that does not interact with the intestinal Na⁺-glucose cotransporter, ³H appeared in plasma, an indication that this stereoisomer of glucose was absorbed. We used ³H levels in plasma and excreta in a pharmacokinetic model to calculate L-glucose extraction efficiency (i.e., the percent absorbed). Calculated mean extraction efficiency for the passively absorbed L-glucose averaged 91% ± 23%. Our finding of considerable passive absorption reconciles the in vitro and in vivo results for D-glucose absorption and is in concert with results from five other avian species. The passive pathway appears to provide birds with an absorptive process that can respond quickly to changing luminal concentration and that is energetically inexpensive to maintain and modulate in real time but that may bear a cost. Less discriminate passive absorption might increase vulnerability to toxins and thus constrain foraging behavior and limit the breadth of the dietary niche.

Intestinal Nutrient Uptake Measurements and Tissue Damage: Validating the Everted Sleeves Method

The reliability of methods for nutrient uptake measurements across the intestinal epithelium relies on the integrity of the mucosal epithelium and the enterocytes. We tested effects of tissue handling during the “everted sleeves method” on the length of intestinal villi, the surface magnification, the circumference of the gut, and the thickness of the muscle layer in sunbirds (Nectarinia osea), chicken (Gallus gallus), and mice (Mus domesticus). The sunbird has thin and delicate intestinal villi that are greatly affected by the everted sleeves method. After eversion and incubation, villi lost 30% of their original length. The severe tissue damage coincides with uptake measurements for glucose that were an order of magnitude lower than in other nectar‐feeding (nectarivorous) birds of similar body size. Tissue handling during the everted sleeves method had significant effects on morphometric parameters of chicken and mouse intestines, but on a light‐microscopical level, the tissue integrity and the cytology of the enterocytes were not altered. Therefore, we think that the everted sleeves method renders reliable and reproducible measurements of nutrient uptake in those species. We conclude that a histological evaluation is necessary to assess the reliability of the method before it is applied to adults or to the developmental stage of any species.

Is Diet Shifting Facilitated by Modulation of Intestinal Nutrient Uptake? Test of an Adaptational Hypothesis in Yellow-Rumped Warblers

Yellow-rumped warblers (Dendroica coronata) are one of many avian species that change their diet seasonally. Using them, we tested the predictions that uptake of D-glucose and the amino acid L-leucine will increase as dietary levels of carbohydrate and protein, respectively, are increased and that mediated uptake capacity of the entire small intestine will match nutrient loads from daily food intake. Birds were fed three semisynthetic diets, formulated from fruit, insects, or seeds, for 7 d. Mediated D-glucose uptake in vitro was affected by diet, but contrary to our a priori prediction, fruit eaters eating the diet highest in carbohydrates had the lowest uptake rate. Na⁺-dependent L-leucine uptake at a low concentration (0.01 mmol L⁻¹) was higher in insect and seed eaters, which is consistent with the prediction of adaptation to dietary protein, though dietary fat may also play a role. Mediated D-glucose uptake summed over small intestine length could explain only a small percentage of the estimated whole-animal absorption rate. We thus reject the predictions for carbohydrate but suggest an alternative interpretation of our results that is consistent with economical design.

Do northern bobwhite quail modulate intestinal nutrient absorption in response to dietary change? A test of an adaptational hypothesis☆

Abstract We acclimated northern bobwhite quail ( Colinus virginianus ) to either chow (high carbohydrate/low protein) or crickets (low carbohydrate/high protein) and tested predictions of hypotheses based on the premise of the economical design of animals. The adaptive modulation hypothesis predicts that d -glucose uptake would be higher and l -proline uptake lower in bobwhites acclimated to chow. The spare capacity hypothesis predicts that the capacity to absorb d -glucose actively will exceed the estimated nutrient load from daily food intake. There was no significant dietary effect on intestinal d -glucose ( P = 0.8) and l -proline ( P = 0.7) uptake rates measured in vitro using the everted sleeve technique. In chow eaters maximal mediated d -glucose uptake summed along the entire length of intestine (53 cm) was far too low (7.2 mmol/d) to explain observed rates of glucose absorption in vivo (>35 mmol/d). Hence, both predictions were falsified. In vitro uptake may not be an appropriate measure of the intestines absorptive capacity because it does not measure possibly important pathways of passive absorption. There is increasing evidence that substantial passive glucose absorption occurs in some birds. If passive absorption predominates the adaptive modulation hypothesis might not apply.

The effects of season and dietary salt content on body temperature daily rhythms of common spiny mice from different micro-habitats

We compared body temperature (T(b)) daily rhythms in two populations of common spiny mice, Acomys cahirinus, during summer and winter months in relation to increasing dietary salt content. Mice were collected from the North and South facing slopes (NFS and SFS) of the same valley, that are exhibiting mesic and xeric habitats, respectively. During the summer, whilst mice were offered a water source containing 0.9% NaCl, SFS individuals had T(b) peak values at 24:00, whereas NFS individuals had peak values at 18:00. When the salinity of the water source was increased, from 0.9 to 2.5% and then 3.5%, the difference between maximal and minimal T(b) of both populations increased. In addition, with increased salinity, the T(b) daily peak of SFS mice shifted to 18:00. During the winter, the mean daily T(b) values of both populations of mice were lower than during the summer. At 0.9% salinity, the NFS mice exhibited a daily T(b) variation with a peak at the beginning of the night. However, we did not detect any significant variation in daily T(b) in the SFS mice. At 2.5% salinity, the difference between the mean daily T(b) of mice from the two slopes increased. In winter we were unable to increase the salinity to 3.5% as the animals began to lose weight rapidly. We suggest that common spiny mice that inhabit these two micro-habitats are forming two discrete populations that respond differently to the environmental pressures prevailing in each habitat, by evolving different physiological capacities.

Differential osmoregulatory capabilities of common spiny mice ( Acomys cahirinus ) from adjacent microhabitats

The osmoregulatory function of common spiny mice Acomys cahirinus living on opposite slopes of the lower Nahal Oren (‘Evolution Canyon’) on mount Carmel, Israel, was investigated by increasing the salinity of the water source whilst maintaining a high-protein diet. The southern-facing slope (SFS) of this canyon differs from the northern-facing slope (NFS) as it receives considerably more solar radiation and consequently forms a more xeric, sparsely vegetated habitat. During the summer, mice living on the two opposite slopes significantly differed in their urine osmolality, which also increased significantly as dietary salinity increased. Offspring of wild-captured mice, born in captivity, and examined during the winter, continued to show a difference in osmoregulatory function depending on the slope of origin. However, they differed from wild-captured mice, as they did not respond to the increase in dietary salinity by increasing the concentration of their urine, but rather by increasing the volume of urine produced. This study shows that A. cahirinus occupying different microhabitats may exhibit differences in their ability to concentrate urine and thus in their ability to withstand xeric conditions. We suggest that they may also differ genetically, as offspring from the NFS and SFS retain physiological differences, but further studies will be needed to confirm this hypothesis.

RETENTION TIME OF DIGESTA IN INSECTIVOROUS LIZARDS: A COMPARISON OF METHODS AND SPECIES

Abstract We measured retention time in the six-lined racerunner, Cnemidophorus sexlineatus, using three different methods simultaneously. This enables us to compare methods, assess retention time of various phases of the lizard’s digesta, and compare the data with other studies, species and methods. Our study reveals that: (1) Total mean retention time for C. sexlineatus was 20.1–23.7 h, the shortest TMRT measures for insectivorous lizards. (2) There was no detectable separation of solid, aqueous, or lipid phases in the digesta of the lizard, probably due to the rapid transit time relative to the frequency of defecation. Studies of lizards with greater retention times indicate separation of liquid and solid phases, but have not tested phase specificity of the markers. Separation of lipid and aqueous phases is important, as was reported before for certain mammals and birds. This is the first study to look for separation of lipid and aqueous phases in reptiles.