Abstract
A major area of interest in comparative physiology has been to understand how animals cope with changing environmental demands in time and space. The digestive system has been identified as one of the more sensitive systems to changes in environmental conditions. However, most research on this topic has evaluated these effects during peak energetic demands, which do not allow for evaluation of the dynamics of the digestive response along a more natural continuous gradient of environmental conditions. We examined phenotypic flexibility in digestive responses of the leaf-eared mouse Phyllotis darwini to increments in total energy demands (via sequential exposure to 26, 12 and 0°C). Additionally, we evaluated the effect of a moderate energy demand (12°C) over three different time periods (7, 17 and 27 days) on digestive traits. Moderate increases in energy demand were associated with changes in the distribution of digesta in the gut, whereas higher increases in energy demand involved increases in the tissue mass of digestive organs. Time-course analysis showed that at 12°C practically all digestive variables reached stable values within 7 days, which is in agreement with empirical data and theoretical deductions from cellular turnover rates. We conclude that although the input of energy and nutrients into the digestive tract is typically periodic, many aspects of digestive physiology are likely to be flexible in response to environmental variability over both short-term (daily) and long-term (seasonal) time scales.
Similar content being viewed by others
Abbreviations
- DDMI:
-
Digestible dry-matter intake
- DM:
-
Dry mass
- DMD:
-
Apparent dry-matter digestibility
- E:
-
Faecal output
- HD:
-
High demand
- I:
-
Food intake
- MD:
-
Moderate demand
- N:
-
Nitrogen
- RCC:
-
Relative amount of digesta in a digestive organ
- T:
-
Thermoneutrality
- Ta:
-
Ambient temperature
- TT:
-
Turnover time
- V:
-
Total amount of digesta in the gut
References
Bacigalupe LD, Bozinovic F (2002) Design, limitation and sustained metabolic rate: lessons from small mammals. J Exp Biol 205:2963–2970
Bacigalupe LD, Rezende EL, Kenagy GJ, Bozinovic F (2003) Activity and space use by degus: a trade-off between thermal conditions and food availability? J Mammal 84:311–318
Bozinovic F, Veloso C, Rosenmann M (1988) Cambios del tracto digestivo de Abrothrix andinus (Cricetidae): efecto de la calidad de dieta y requerimientos de energía. Rev Chil Hist Nat 61:245–251
Bozinovic F, Novoa F, Sabat P (1997) Feeding and digesting fiber and tannins by the Herbivorous rodent, Octodon degus (Rodentia: Caviomorpha). Comp Biochem Physiol 118A:625–630
Derting TL, Bogue BA (1993) Responses of the gut to moderate energy demands in a small herbivore (Microtus pennsylvanicus). J Mammal 74:59–68
Diamond JM, Karasov WH (1983) Trophic control of the intestinal mucosa. Nature 304:18
Dykstra CR, Karasov WH (1992) Changes in gut structure and function of house wrens (Troglodytes aedon) in response to increased energy demands. Physiol Zool 65:422–442
Green DA, Millar JS (1987) Changes in gut dimensions and capacity of Peromyscus maniculatus relative to diet quality and energy needs. Can J Zool 65:2159–2162
Gross JE, Wang Z, Wunder BA (1985) Effects of food quality and energy needs: changes in gut morphology and capacity of Microtus ochrogaster. J Mammal 66:661–667
Hammond KA, Wunder BA (1991) The role of diet quality and energy need in the nutritional ecology of a small herbivore, Microtus ochrogaster. Physiol Zool 64:541–567
Hammond KA., Wunder BA (1995) Effect of cold temperatures on the morphology of gastrointestinal tracts of two microtine rodents. J Mammal 76:232–239
Hammond KA, Roth J, Janes DN, Dohm MR (1999) Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 72:613–622
Horwitz W (1980) Official methods of analysis. Association of Official Analytical Chemists, Washington, DC
Karasov WH, Pond RS III, Solberg DH, Diamond J (1983) Regulation of proline and glucose transport in mouse intestine by dietary substrate levels. Proc Natl Acad Sci USA 80:7674–7677
Konarzewski M, Diamond J (1994) Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiol Zool 67:1186–1212
Levey DJ, Duke GE (1992) How do frugivores process fruit? Gastrointestinal transit and glucose absorption in cedar waxwings (Bombycilla cedrorum). Auk 109:722–730
Levey DJ, Martínez del Río C (1999) Test, rejection, and reformulation of a chemical reactor-based model of gut function in a fruit-eating bird. Physiol Biochem Zool 72:369–383
Loeb SC, Schwab RG, Demment MW (1991) Responses of pocket ghophers (Thomomys bottae) to changes in diet quality. Oecologia 86:542–551
Lopez-Calleja MV, Bozinovic F, Martínez del Río C (1997) Effects of sugar concentration on hummingbird feeding and energy use. Comp Biochem Physiol 118A:1291–1299
Martínez del Río C, Brugger KE, Ríos JL, Vergara ME, Witmer M (1995) An experimental and comparative study of dietary modulation of intestinal enzymes in European starlings (Sturnus vulgaris). Physiol Zool 68:490–511
McDevitt RM, Speakman JR (1994) Central limits to sustainable metabolic rate have no role in a cold acclimation of the short-tailed field vole (Microtus agrestis). Physiol Zool 67:1117–1139
McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol 128A:579–593
Meserve PL (1981) Trophic relationship among small mammals in a Chilean semiarid thorn scrub community. J Mammal 62:304–314
Moss R (1974) Winter diets, gut lengths, and interespecific competition in Alaskan Ptarmigan. Auk 91:737–746
Nagy TR, Negus NC (1993) Energy acquisition and allocation in male collared lemmings (Dicrostonyx groenlandicus): effects of photoperiod, temperature, and diet quality. Physiol Zool 66:537–560
Naya DE, Bozinovic F (2004) Digestive phenotypic flexibility in post-metamorphic amphibians: studies on a model organism. Biol Res 37:365–370
Nespolo RF, Opazo JC, Bozinovic F (2001) Thermal acclimation and non-shivering thermogenesis in three species of South American rodents: a comparison between arid and mesic habitats. J Arid Environ 48:581–590
Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimatation. J Exp Biol 205:2697–2703
Pei Y-X, Wang D-H, Hume ID (2001) Selective digesta retention and coprophagy in Brandt’s vole (Microtus brandti). J Comp Physiol B 171:457–464
Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233
Piersma T, Lindstrom A (1997) Rapid reversible changes in organ size as a component of adaptative behaviour. Trends Ecol Evol 12:134–138
Sabat P, Bozinovic F (2000) Digestive plasticity and the cost of acclimation to dietary chemistry in the omnivorous leaf-eared mouse Phyllotis darwini. J Comp Physiol B 170:411–417
Sabat P, Bozinovic F, Zambrano F (1995) Role of dietary substrates on intestinal disaccharidases, digestibility and energetics in the insectivorous mouse-opossum (Thylamys elegans). J Mammal 76:603–611
Scheiner SM (2002) Selection experiments and the study of phenotypic plasticity. J Evol Biol 15:889–898
Schwaibold U, Pillay N (2003) The gut morphology of the African ice rat, Otomys sloggetti robertsi, shows adaptation to cold environments and sex-specific season variation. J Comp Physiol B 173:653–659
Sibly RM (1981) Strategies of digestion and defecation. In: Towsend CR, Calow P (eds) Physiological ecology: an evolutionary approach to resource use. Blackwell, Oxford, pp 109–139
Starck JM (1999) Structural flexibility of the gastro-intestinal tract of vertebrates—implications for evolutionary morphology. Zool Anz 238:87–101
Stearns C (1989) The evolutionary significance of phenotypic plasticity. Bioscience 39:436–445
Toloza E, Lam M, Diamond J (1991) Nutrient extraction by cold-exposed mice: a test of digestive safety margins. Am J Physiol 261:G608–G620
Acknowledgements
Ian Hume provided valuable comments. DEN and DMB acknowledge fellowships from the Dirección General de Posgrado de la Pontificia Universidad Católica de Chile (DIPUC, Chile) and Comisión Nacional de Investigación Científica y Tecnológica (CONICYT, Chile). LDB is a post-doc fellow from the Center for Advances Studies in Ecology and Biodiversity (CASEB, Program 1). This work was funded by Fondo Nacional de Ciencia y Tecnología FONDAP 1501-0001 (Program 1). All experiments were conducted according to current Chilean law, and under permit SAG 698. This paper is dedicated to the memory of Dr Mario Rosenmann.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D Hume
Rights and permissions
About this article
Cite this article
Naya, D.E., Bacigalupe, L.D., Bustamante, D.M. et al. Dynamic digestive responses to increased energy demands in the leaf-eared mouse (Phyllotis darwini). J Comp Physiol B 175, 31–36 (2005). https://doi.org/10.1007/s00360-004-0459-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-004-0459-8