Effect of fasting on the structure and function of the gastrointestinal tract of house sparrows (Passer domesticus)

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Abstract

Starvation is a condition that often affects animals in nature. The gastrointestinal tract is the organ system displaying the most rapid and dramatic changes in response to nutrient deprivation. To date, little is known about starvation phases and effects on the organ morphology and digestive function in small passerine birds. In this study, we determined the phases of starvation and examined the effect of final stage of starvation in the organ morphology and, intestinal histology and enzymatic function in the small intestine. Our results show the three phases of the classical model of fasting in a shorter period of time. The mass of heart, pancreas, stomach, small intestine and liver of long-term fasted birds was reduced between 20 and 47%. The mass decrease in small intestine was correlated with reduction in small intestinal histology: perimeter, mucosal thickness, villus height and width. In contrast, the enzyme activity of sucrase–isomaltase and aminopeptidase-N in enterocytes, all expressed per μg of protein, was higher in long-term fasted birds than fed animals. This suggest that, while autophagy of digestive organs is induced by starvation, consistent with phenotypic plasticity, the activity of sucrase–isomaltase and aminopeptidase-N remains high, probably as an anticipatory strategy to optimize digestion at re-feeding time.

Introduction

Starvation is an ecological relevant situation, in which animals do not have enough nutrients to feed on, as a result of some extrinsic limitation on food resources. In nature, starvation occurs as a natural event and can vary widely in frequency and duration, i.e.: rainstorm, snowstorm (McCue, 2010). When animals are exposed to changes in nutrient quality and quantity, they exhibit adaptive biochemical., physiological and molecular responses such as a reduction in body weight and visceral organ mass, atrophy of intestinal mucosa, immune dysfunction and decrease of activity enzyme, among others (Ferraris and Carey, 2000, Chappell et al., 2003, Starck, 2003, Houston et al., 2007).

The response to food deprivation in birds and mammals has been characterized by three consecutive phases defined by progressive metabolic and physiological changes (Wang et al., 2006, McCue, 2010). Phase I occurs immediately after the last food has been absorbed at the small intestine. It is characterized by both the use of liver glycogen stores and a significant body mass reduction in a short time. Phase II is based on the energy economization and oxidation of lipids. Since lipids have high amount of energy, weight loss is slow during this stage. Finally, at phase III, when lipid deposits are depleted, muscle protein catabolism begins combined with a decrease in protein synthesis. As a result of protein degradation, the rate of body mass loss increases along with nitrogenous waste (uric acid) production (Wang et al., 2006). The first objective of this work was to characterize the degradation response to starvation in the house sparrows by biochemical parameters in plasma and body mass changes. We expected to see the same three phases of the classical model of fasting but in a shorter period of time, since small animals are more susceptible to the complete absence of food than those of a larger size. The increased energetic demand to keep homeostasis of the body during starvation is reflected in the down regulation of tissue and organ mass (Bauchinger et al., 2005). In vertebrates, the digestive system is the most affected and displays dramatic changes (Ferraris and Carey, 2000, Starck, 2003, McCue, 2010). Consequently, morphological studies during fasting have showed changes in villus length and thickness, as well as in enterocyte phenotype. Besides, generative components (crypts) of the mucosa are preferentially preserved in comparison to the absorptive part (villi) (Dunel-Erb et al., 2001, Karasov et al., 2004).

The second objective was to evaluate the effects of long period of food deprivation (phase III of starvation) on organ size and histological parameters in small intestine (perimeter, mucosal layer, villus length and crypt size).

It is known that the structure and function of the gastrointestinal tract in vertebrates is flexible. Previous studies have been performed mainly in mammals, poultry or migratory birds (Yamauchi et al., 1997, Ferraris and Carey, 2000, Fassbinder-Orth and Karasov, 2006, Wang et al., 2006), but there is little information about the mechanisms (i.e. enzyme activity, intestinal absorption, gene expression) involved in the energy administration process in small non-migratory passerine birds during fasting (Karasov and Martínez del Rio, 2007). A reason to study digestive changes in small non-migratory passerine birds in response to a total lack of food is because migrant birds may be under a selective pressure for fasting, (Lindstrom and Alerstam, 1992). In addition, flexibility of the digestive capacity during fasting in non-migrant birds could play a significant role in the economization of energy use (Klaassen et al., 1997). Several studies in mammals had shown a down regulation of enzyme activity during starvation (Holt and Yeh, 1992, Ihara et al., 2000) because the activities of different digestive enzymes and nutrient transporters are regulated positively by their substrate concentration (Sanderson and Naik, 2000, Ferraris, 2001). In contrast, there is little information about this process in birds, in poultry and passerine migratory birds (Dendroica coronate) with 54% of food restriction, but not total restriction, the activity of digestive enzymes decreases (Lee et al., 2002, Fassbinder-Orth and Karasov, 2006). On the other hand, in poultry, there is an interesting pattern of plasticity of the intestinal enzyme activities in response to diet, where variations in activity of disaccharidases, but not aminopeptidase-N, in the small intestine have been detected (Biviano et al., 1993, Ciminari, 2011). In contrast, passerine birds modulated the aminopeptidase-N activity in response to diet but disaccharidases activity remained invariable (Caviedes-Vidal et al., 2000, Ciminari, 2011).

The third goal was to investigate the effects of long period of food deprivation (phase III of starvation) on the hydrolytic enzymes (sucrose–isomaltase and aminopeptidase-N) activity in the enterocytes along the intestine. In addition we investigated a parallel change between mRNA of sucrose–isomaltase and activity, to integrate molecular and cellular level.

Section snippets

Animal care and housing

Adult house sparrows (Passer domesticus) were captured with live traps near the Universidad Nacional de San Luis Campus (San Luis, Argentina). The birds were housed in cages (40 × 25 × 25 cm) indoors under relatively constant environmental conditions (23 ± 1 °C) on a photoperiod of 14:10 h (light:dark) with food and water ad libitum (seeds supplied with vitamins and minerals). Animals were acclimated to laboratory conditions for two weeks prior to use in experiments. Animal care and trial protocols

Body mass loss and biochemical changes at phases of fasting

In order to explain the changes in body mass (BM) throughout the fasting period and their correspondence with the classical model of three phases, we analyzed total BM loss and rate of BM loss (experiment 1). Fasted animals (n = 7) lost an average of 17% of initial BM (initial BM: 25.66 ± 0.288; final BM: 21.18 ± 0.29, p < 0.001). During the first h of fasting (until 4 h, phase I) the rate of BM loss (mg/g * h) was markedly reduced (p < 0.002); from intermediate h (~ 12 h to 28 h, phase II) the rate of BM loss

Discussion

According with the first objective of this study the three metabolic phases of fasting were established in house sparrows; this pattern is consistent with the classic profile of the three stages of fasting previously described in larger mammals and birds (Alonso-Alvarez and Ferrer, 2001, Wang et al., 2006). Based on blood sampling times, the time limits (in hours) of the phases of fasting in house sparrows (Fig. 1) were established as follows: phase I is characterized by the use of nutrients

Acknowledgements

We thank Claudia Gatica Sosa y Guido Fernández Marinone for their logistic support in the laboratory. Samanta Funes is a doctoral fellowship from CONICET. The authors thank to Dr. William Karasov (University of Wisconsin) and Dr. Sergio Alvarez (UNSL and Virginia Commonwealth University) for his thorough and critical reading of the manuscript. This work was supported by PIP CONICET and CYT-UNSL (22/Q047) to Juan Gabriel Chediack and FONCYT (PICT 2007-01320) and CYT-UNSL (22/Q751) to Enrique

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