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Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus)

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Abstract

In the context of evolution and ecology, there is a trade-off between the benefits of processing food through a digestive system with specific phenotypic attributes and the cost of maintaining and carrying the digestive system. In this study, we tested the hypothesis that digestive modulations at several levels can match each other to meet the energy and nutrient demands of Mongolian gerbils, a small granivorous rodent species, by acclimating them to a high-quality diet diluted with alfalfa powder. Mongolian gerbils on the diluted diet maintained metabolizable energy intake by an integrated processing response (IPR), which included increases in dry matter intake, gut capacity and rate of digesta passage after 2-weeks of acclimation. Down-regulation of hydrolytic enzyme activity in the intestinal brush-border membrane supported the adaptive modulation hypothesis. The absence of up-modulation of summed enzyme hydrolytic capacity on the diluted diet indicated that greater mass of small intestine on a high-fibre diet is not a direct indicator of digestive or absorptive capacity. Changes in mass of vital organs and carcass suggested that the amount of energy allocated to various organs and hence physiological functions was regulated in response to diet shift.

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Reference

  • Afik D, Darken BW, Karasov WH (1997) Is diet shifting facilitated by modulation of intestinal nutrient uptake? Test of an adaptational hypothesis in yellow-rumped warblers. Physiol Zool 70:213–221

    PubMed  CAS  Google Scholar 

  • Batzli GO, Broussard AD, Oliver RJ (1994) The integrated processing response in herbivorous small mammals. In: Chivers DJ, Langer P (Eds) The digestive system in mammals: food, form and function, Cambridge University Press, Cambridge, pp 324–336

    Google Scholar 

  • Bozinovic F (1995) Nutritional energetics and digestive responses of an herbivorous rodent (Octodon degus) to different levels of dietary fiber. J Mammal 76:627–637

    Article  Google Scholar 

  • Buddington RK, Chen JW, Diamond JM (1991) Dietary regulation of intestinal brush-border sugar and amino acid transport in carnivores. Am J Physiol 261:R793–R801

    PubMed  CAS  Google Scholar 

  • Castle KT, Wunder BA (1995) Limits to food intake and fiber utilization in the prairie vole, Microtus ochrogaster: effects of food quality and energy need. J Comp Physiol B 164:609–617

    Article  Google Scholar 

  • Caviedes-Vidal E, Karasov WH (1996) Glucose and amino acid absorption in house sparrow intestine and its dietary modulation. Am J Physiol 271:R561–R568

    PubMed  CAS  Google Scholar 

  • Dahlqvist A (1984) Assay of intestinal dissaccharidases. Scan J Clin Invest 44:69–172

    Google Scholar 

  • Derting TL, Bogue BA (1993) Responses of the gut to moderate energy demands in a small herbivore (Microtus pennsylvanicus). J Mammal 74:59–68

    Article  Google Scholar 

  • Derting TL, Compton S (2003) Immune response, not immune maintenance, is energetically costly in wild white-footed mice (Peromyscus leucopus). Physiol Biochem Zool 76:744–752

    Article  PubMed  Google Scholar 

  • Derting TL, Hornung CA (2003) Energy demand, diet quality, and central processing organs in wild white-footed mice (Peromyscus leucopus). J Mammal 84:1381–1398

    Article  Google Scholar 

  • Diamond JM (1991) Evolutionary design of intestinal nutrient absorption: enough but not too much. News Physiol Sci 6:92–96

    Google Scholar 

  • Diamond JM, Karasov WH (1983) Trophic control of the intestinal mucosa. Nature 304:18

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Ferraris RP, Diamond JM (1989) Specific regulation of intestinal nutrient transporters by their dietary substrates. Annu Rev Physiol 51:125–141

    Article  PubMed  CAS  Google Scholar 

  • Ferraris RP, Lee PP, Diamond JM (1989) Origin of regional and species differences in intestinal glucose uptake. Am J Physiol 257:G689–G697

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gross JE, Wang ZW, Wunder BA (1985) Effects of food quality and energy needs: changes in gut morphology and capacity of Microtus ochrogaster. J Mammal 66:661–667

    Article  Google Scholar 

  • Hammond KA, Diamond JM (1992) An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiol Zool 65:952–977

    Google Scholar 

  • Hammond KA, Janes DN (1998) The effects of increased protein intake on kidney size and function. J Exp Biol 201:2081–2090

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Hammond KA, Konarzewski M, Torres RM, Diamond JM (1994) Metabolic ceilings under a combination of peak energy demands. Physiol Zool 67:1476–1506

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hume ID, Morgan ID, Kenagy GJ (1993) Digesta retention and digestive performance in sciurid and microtine rodents: effects of hindgut morphology and body size. Physiol Zool 66:396–411

    Google Scholar 

  • Johnson MS, Thomson SC, Speakman JR (2001) Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus. J Exp Biol 204:1925–1935

    PubMed  CAS  Google Scholar 

  • Kanarek RB, Ogilby JD, Mayer J (1977) Effects of dietary caloric density on feeding behavior in Mongolian gerbils (Meriones unguiculatus). Physiol Behav 19:497–501

    Article  PubMed  CAS  Google Scholar 

  • Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (Ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 61–84

    Google Scholar 

  • Karasov WH, Diamond JM (1983) Adaptive regulation of sugar and amino acid transport by vertebrate intestine. Am J Physiol 245:G443–G462

    PubMed  CAS  Google Scholar 

  • Karasov WH, Diamond JM (1988) Interplay between physiology and ecology in digestion. BioScience 38:602–611

    Article  CAS  Google Scholar 

  • Karasov WH, Hume ID (1997) Vertebrate gastrointestinal system. In: Dantzler W (ed) Handbook of comparative physiology. American Physiological Society, Bethesda, pp 409–480

  • Karasov WH, Pond RS III, Solberg DH, Diamond JM (1983) Regulation of proline and glucose transport in mouse intestine by dietary substrate levels. Proc Natl Acad Sci 80:7674–7677

    Article  PubMed  CAS  Google Scholar 

  • Król E, Speakman JR (2003) Limits to sustained energy intake. VII. Milk energy output in laboratory mice at thermoneutrality. J Exp Biol 206:4267–4281

    Article  PubMed  Google Scholar 

  • Lentle RG, Stafford KJ, Hume ID (2004) A comparison of the gross gastrointestinal morphology of genetically-similar tammar wallabies (Macropus eugenii) from different nutritional environments. Aust J Zool 52:437–445

    Article  Google Scholar 

  • Maroux S, Louvard D, Baratii J (1973) The aminopeptidase from hog intestinal brush-border. Biochim Biophys Acta 321:282–295

    PubMed  CAS  Google Scholar 

  • Martínez del Río C (1990) Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol Zool 63:987–1011

    Google Scholar 

  • Martínez del Río C, Brugger KE, Rios JL, Vergara ME, Witmer M (1995) An experimental and comparative study of dietary modulation of intestinal enzymes in the European starling (Sturnus vulgaris). Physiol Zool 68:490–511

    Google Scholar 

  • McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A 128:579–593

    CAS  Google Scholar 

  • Munn AJ, Banks P, Hume ID (2006) Digestive plasticity of the small intestine and the fermentative hindgut in a marsupial herbivore, the tammar wallaby (Macropus eugenii). Aust J Zool 54:287–291

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Naya DE, Bacigalupe LD, Bustamante DM, Bozinovic F (2005) Dynamic digestive responses to increased energy demands in the leaf-eared mouse (Phyllotis darwini). J Comp Physiol B 175:31–36

    Article  PubMed  Google Scholar 

  • Pei YX, Wang DH, Hume ID (2001a) Selective digesta retention and coprophagy in Brandt’s vole (Microtus brandti). J Comp Physiol B 171:457–464

    Article  PubMed  CAS  Google Scholar 

  • Pei YX, Wang DH, Hume ID (2001b) Effects of dietary fibre on digesta passage, nutrient digestibility, and gastrointestinal tract morphology in the granivorous Mongolian gerbil (Meriones unguiculatus). Physiol Biochem Zool 74:742–749

    Article  PubMed  CAS  Google Scholar 

  • Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96

    Article  CAS  Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  • Piersma T, Lindstrom A (1997) Rapid reversible changes in organ size as a component of adaptative behaviour. Trends Ecol Evol 12:134–138

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sabat P, Novoa F, Bozinovic F, Martínez del Río C (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Zool 71:226–236

    PubMed  CAS  Google Scholar 

  • Sakaguchi E, Itoh H, Uchida S, Horigome T (1987) Comparison of fibre digestion and digesta retention time between rabbits, guinea-pigs and hamsters. Br J Nutr 58:149–158

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Speakman JR, McQueenie J (1996) Limits to sustained metabolic rate: the link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus. Physiol Zool 69:746–769

    Google Scholar 

  • Starck JM (1999a) Phenotypic flexibility of the avian gizzard: rapid, reversible, and repeated changes of organ size in response to changes in dietary fiber content. J Exp Biol 202:3171–3179

    PubMed  Google Scholar 

  • Starck JM (1999b) Structural flexibility of the gastro-intestinal tract of vertebrates. Implications for evolutionary morphology. Zool Anz 238:87–101

    Google Scholar 

  • Starck JM, Rahmaan GH (2003) Phenotypic flexibility of structure and function of the digestive system of Japanese quail. J Exp Biol 206:1887–1897

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wunder BA (1992) Morphophysiological indicators of the energy state of small mammals. In: Tomasi TE, Horton TH (eds) Mammalian energetics: interdisciplinary views of metabolism and reproduction. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, pp 83–104

    Google Scholar 

  • Xia WP, Zhong WQ (1966) The successions and interactions of the rodent and plant communities of abandoned fields in desert steppe at Chagan-AoBao, Inner Mongolia (in Chinese with English abstract). Acta Zool Sin 18:199–208

    Google Scholar 

  • Young Owl M, Batzli GO (1998) The integrated processing response of voles to fibre content of natural diets. Funct Ecol 12:4–13

    Article  Google Scholar 

  • Zhang ZQ (2005) Seasonal changes in thermogenesis, energy budgets and immune function in Mongolian gerbils (Meriones unguiculatus). Unpublished PhD Thesis, Chinese Academy of Sciences, Beijing

  • Zhao ZJ (2006) Roles of photoperiod and diet quality in the regulation of energy metabolism, body mass, and thermogenic capacity in Brandt’s voles and Mongolian gerbils. Unpublished PhD Thesis, Cihinese Academy of Sciences, Beijing

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Acknowledgments

We thank Professor Ian D Hume and two anonymous reviewers for their constructive comments and suggestions for improving the manuscript.Thanks to Dr. T Derting for reading an earlier draft of this manuscript and improving the English expression. We are grateful to Zhao Zhi-Jun and Jing Bo-Bin for their help with animal care and dissection and to Professor Enrique Caviedes-Vidal for his help for assaying enzyme activity. This work was partly supported by grants from the National Natural Science Foundation of China (No. 30430140 and 30570230) to DHW and the CAS Innovative Research International Partnership Project (CXTDS2005-4).

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Authors and Affiliations

  1. State Key Laboratory of Integrated Management for Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuan Xilu, Zhongguancun, Haidian, Beijing, 100080, China

    Quan-Sheng Liu & De-Hua Wang

  2. Guangdong Key Laboratory of Integrated Pest Management in Agriculture, Guangdong Entomological Institute, 105 Xin’gang Xilu, Haizhu, Guangzhou, 510260, China

    Quan-Sheng Liu

  3. Graduate School of the Chinese Academy of Sciences, Yuquan Lu, Beijing, 100049, China

    Quan-Sheng Liu

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  1. Quan-Sheng Liu
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  2. De-Hua Wang
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Correspondence to De-Hua Wang.

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Communicated by I.D. Hume.

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Liu, QS., Wang, DH. Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). J Comp Physiol B 177, 509–518 (2007). https://doi.org/10.1007/s00360-007-0149-4

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