Skip to main content
SpringerLink
Log in

Seasonal plasticity of gut morphology and small intestinal enzymes in free-living Mongolian gerbils

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The phenotypic plasticity of the digestive system may determine the diversity of animal diets and, thus, their niche width. This study examines the effects of seasonal fluctuations in food quality and temperature on the gut morphology and the activity of sucrase, maltase, and aminopeptidase-N in the small intestinal brush-border membrane of male Mongolian gerbils (Meriones unguiculatus). Based on the adaptive modulation hypothesis and the principle of optimal gut function design, we hypothesize that the gut size, tissue-specific activity, and total hydrolytic capacity of intestinal digestive enzyme are upregulated in winter and downregulated in summer in response to diet shifts and energy demand in free-living Mongolian gerbils. Various seasonal modulation patterns in digestive enzyme activity in different regions of the small intestines were observed. The results show that male gerbils have the longest and heaviest small intestines in winter. This mechanism may be adapted to increase their food intake during winter. Male gerbils also exhibit the highest tissue-specific and total sucrase, maltase, and aminopeptidase-N activity in winter and in spring. Seasonal modulations are more distinct in the jejunum than in the duodenum and the ileum of the small intestines. The digestive phenotypic flexibility of male gerbils effectively corresponded with seasonal diet shifts and temperature fluctuations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Afik D, Karasov WH (1995) The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76:2247–2257

    Article  Google Scholar 

  • Afik D, Caviedes-Vidal E, Martínez del Rio C, Karasov WH (1995) Dietary modulation of intestinal hydrolytic enzymes in yellow-rumped warblers. Am J Physiol 269:R413–R420

    PubMed  CAS  Google Scholar 

  • Buddington RK (1992) Intestinal nutrient transport during ontogeny of vertebrates. Am J Physiol 263:R503–R509

    PubMed  CAS  Google Scholar 

  • Caviedes-Vidal E, Afik D, Martínez del Rio C, Karasov WH (2000) Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis. Comp Biochem Physiol A 125:11–24

    CAS  Google Scholar 

  • Cezard JP, Broyart JP, Cuisinier-Gleizes P, Mathieu H (1983) Sucrase–isomaltase regulation by dietary sucrose in the rat. Gastroenterol 84:18–25

    CAS  Google Scholar 

  • Chen D, Li YP (2000) Dietary study of Mongolian gerbils population in the Tumete Plain, Inner Mongolia. Inn Mong Prev Med 25:76–77

    Google Scholar 

  • Christians JK (1999) Controlling for body mass effects: is part-whole correlation important? Physiol Biochem Zool 72:250–253

    Article  PubMed  CAS  Google Scholar 

  • Ciminari E, del Valle Moyano G, Chediack JG, Caviedes-Vidal E (2005) Feral pigeons in urban environments: dietary flexibility and enzymatic digestion? Rev Chil Hist Nat 78:267–279

    Article  Google Scholar 

  • Dahlqvist A (1984) Assay of intestinal disaccharidases. Scan J Clin Lab Invest 44:169–172

    Article  CAS  Google Scholar 

  • del Valle JC, López Mañanes AA, Busch C (2004) Phenotypic flexibility of digestive morphology and physiology of the South American omnivorous rodent Akodon azarae (Rodentia: Sigmodontinae). Comp Biochem Physiol A 139:503–512

    Article  Google Scholar 

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

    Article  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 

  • Derting TL, Noakes EB (1995) Seasonal changes in gut capacity in the white-footed mouse (Peromyscus leucopus) and the meadow vole (Microtus pennsylvanicus). Can J Zool 73:243–252

    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 

  • Goda T, Yamada K, Bustamante S, Koldovsky O (1983) Dietary-induced rapid decrease of microvillar carbohydrase activity in rat jejuno ileum. Am J Physiol 245:G418–G423

    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 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

    Article  Google Scholar 

  • Hammond KA, Wunder BA (1995) Effect of cold temperatures on the morphology of gastrointestinal tracts of two microtine rodents. J Mammal 76:232–239

    Article  Google Scholar 

  • Hammond KA, Konauewski M, Torres RM, Diamond JM (1994) Metabolic ceilings under a combination of peak energy demands. Physiol Zool 67:1479–1506

    Google Scholar 

  • Hernandez A, Martínez del Rio C (1992) Intestinal disaccharidases in five species of phyllostomid bats with contrasting feeding habits. Comp Biochem Physiol B 103:105–111

    Article  PubMed  CAS  Google Scholar 

  • Hume ID (1989) Optimal digestive strategies in mammalian herbivores. Physiol Zool 62:1145–1163

    Google Scholar 

  • Karasov WH (1992) Tests of the adaptive modulation hypothesis for dietary control of intestinal nutrient transport. Am J Physiol 263(3):R496–R502

    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 and Hall, New York, pp 61–84

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

    Google Scholar 

  • Karasov WH, Martínez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Karasov WH, McWilliams SR (2005) Digestive constraints in mammalian and avian ecology. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 87–112

    Google Scholar 

  • Karasov WH, Martínez del Rio C, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93

    Article  PubMed  CAS  Google Scholar 

  • Khokhlova IS, Degen AA, Kam M (1995) Body size, gender, and seed husking and energy requirements in two species of desert gerbilline rodents, Meriones crassue and Gerbillus henleyi. Funct Ecol 9:720–724

    Article  Google Scholar 

  • Koldovsky O (1981) Developmental, dietary and hormonal control of intestinal disaccharidases in mammals (including man). In: Randle JP, Steiner DF, Shelan WJ, Whelan WP (eds) Carbohydrate metebolism and its disorders. Academic, London, pp 418–522

    Google Scholar 

  • Levey DJ, Place AR, Rey PJ, Martínez del Rio C (1999) An experimental test of dietary enzyme modulation in pine warblers Dendroica pinus. Physiol Biochem Zool 72:576–587

    Article  PubMed  CAS  Google Scholar 

  • Li XS, Wang DH (2005) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B 175:593–600

    Article  PubMed  CAS  Google Scholar 

  • Liu QS, Wang DH (2007) Effects of diluted diet on phenotypic flexibility of organs morphology and digestive function in Mongolian gerbils (Meriones unguiculatus). J Comp Physiol B 177:509–518

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Zhong WQ, Wan XR, Wang GH (2001) The behavioral characteristics of Mongolian gerbils, Meriones unguiculatus, and the ecological strategies of controlling during autumn harvest. Acta Theriol Sin 21:107–115 (in Chinese with English abstract)

    Google Scholar 

  • Liu H, Wang DH, Wang ZW (2002) Maximum metabolizable energy intake in the Mongolian gerbil (Meriones unguiculatus). J Arid Environ 52:405–411

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Martínez del Rio C, Brugger KE, Rios JL, Vergara ME, Witmer M (1990) An experimental and comparative study of dietary modulation of intestinal enzymes in European starlings (Sturnus vulgaris). Physiol Zool 68:490–511

    Google Scholar 

  • McCarthy DM, Nicholson JA, Kim YS (1980) Intestinal enzyme adaptation to normal diets of different composition. Am J Physiol 239:G445–G451

    PubMed  CAS  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 

  • McWilliams SR, Caviedes-Vidal E, Karasov WH (1999) Digestive adjustments in Cedar Waxwings to high feeding rate. J Exp Zool 283:394–407

    Article  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 

  • Naya DE, Bozinovic F, Karasov WH (2008) Latitudinal trends in digestive flexibility: testing the climatic variability hypothesis with data on the intestinal length of rodents. Am Nat 173(4):122–134

    Article  Google Scholar 

  • 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 acclimation. J Exp Biol 205:2697–2703

    PubMed  Google Scholar 

  • Padilla DK, Adolph SC (1996) Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol 10(1):105–117

    Article  Google Scholar 

  • Pei YX, Wang DH, Hume ID (2001a) Effects of dietary fiber 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 

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

    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 

  • Randolph JC, Cameron GN (2001) Consequences of diet choice by a small generalist herbivore. Ecol Monogr 71:117–136

    Article  Google Scholar 

  • Raul F, Goda T, Gosse F, Koldovsky O (1987) Short-term effect of high-protein/low-carbohydrate diet on aminopeptidase in adult rat jejuno ileum. J Biochem 247:401–405

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sabat P, Lagos JA, Bozinovic F (1999) Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity. Comp Biochem Physiol A 123:83–87

    Article  CAS  Google Scholar 

  • Semenza G, Auricchio S (1989) Small-intestine disaccharidases. In: Scribner CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic basis of inherited disease (II). McGraw Hill, New York, pp 2975–2997

    Google Scholar 

  • Sibly RM (1981) Strategies in digestion and defecation. In: Townsend CR, Calow P (eds) Physiological ecology: an evolutionary approach to resource use. Blackwell Scientific Publications, Oxford, pp 109–139

    Google Scholar 

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

    Google Scholar 

  • Starck JM (2005) Structural flexibility of the digestive system of tetrapods—patterns and processes at the cellular and tissue level. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 175–200

    Google Scholar 

  • Stein RW, Place AR, Lacourse T, Gulielmo CG, Williams TD (2005) Digestive organ sizes and enzyme activity of refueling western sandpipers (Calidris mauri): contrasting effects of season and age. Physiol Biochem Zool 78:434–446

    Article  PubMed  Google Scholar 

  • Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University Press, New York

  • Toloza EM, Lam M, Diamond JM (1991) Nutrient extraction by cold-exposed mice: a test of digestive safety margins. Am J Physiol 261:G608–G620

    PubMed  CAS  Google Scholar 

  • Vonk HJ, Western RH (1984) Comparative biochemistry and physiology of enzymatic digestion. Academic Press, London

    Google Scholar 

  • Wang DH, Wang ZW, Wang YS, Yang JC (2003) Seasonal changes of thermogenesis in Mongolian gerbils (Meriones unguiculatus) and Brandt’s voles (Microtus brandti). Comp Biochem Physiol A 134:S96 (Abstract)

    Google Scholar 

  • Weiss SL, Lee EA, Diamond JM (1998) Evolutionary matches of enzyme and transporter capacities to dietary substrate loads in the intestinal brush border. Proc Natl Acad Sci 95:2117–2121

    Article  PubMed  CAS  Google Scholar 

  • Witmer MC, Martínez del Rio C (2001) The membrane‐bound intestinal enzymes of waxwings and thrushes: adaptive and functional implications of patterns of enzyme activity. Physiol Biochem Zool 74(4):584–593

    Article  PubMed  CAS  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. Acta Zool Sin 18:199–208 (in Chinese with English abstract)

    Google Scholar 

  • Xia WP, Liao CH, Zhong WQ, Sun CL, Tian Y (1982) On the population dynamics and regulation of Meriones unguiculatus in agricultural region north to Yin Mountains, Inner Mongolia. Acta Theriol Sin 2:51–71 (in Chinese with English abstract)

    Google Scholar 

  • Zhang ZB, Wang ZW (1998) Ecology and management of rodent pests in agriculture. Ocean Press, Beijing

  • Zhang ZB, Zhong WQ, Fan NC (2003) Rodent problems and management in the grasslands of China. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) Rats, mice and people: rodent biology and management. ACIAR Monograph, No. 96, 5649, Canberra, pp 316–319

  • Zhong WQ, Zhou QQ, Sun CL (1985) The basic characteristics of the rodent pests on the pasture in Inner Mongolia and the ecological strategies of controlling. Acta Theriol Sin 5:241–249 (in Chinese with English abstract)

    Google Scholar 

Download references

Acknowledgments

We thank three anonymous reviewers for their constructive comments and suggestions for improving the manuscript. We thank Prof. Zhong Wen-Qin, Dr. Liu Wei and Liu Wen-Dong for their logistic support in the field. The work was supported by Grants from the National Natural Science Foundation of China (No. 30625009, 31071930 and 31100297) and partly by projects from Guangdong Provincial Department of Science and Technology (No. 2011B090300039). All experiments were conducted according to current China law.

Author information

Authors and Affiliations

  1. State Key Laboratory of Integrated Management for Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Chaoyang, Beijing, 100101, China

    Quan-Sheng Liu, Zhi-Qiang Zhang & 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. Departamento de Bioquimica y Ciencias Biologicas, Universidad Nacional de San Luis, 5700, San Luis, Argentina

    Enrique Caviedes-Vidal

Authors
  1. Quan-Sheng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhi-Qiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrique Caviedes-Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. De-Hua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to De-Hua Wang.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, QS., Zhang, ZQ., Caviedes-Vidal, E. et al. Seasonal plasticity of gut morphology and small intestinal enzymes in free-living Mongolian gerbils. J Comp Physiol B 183, 511–523 (2013). https://doi.org/10.1007/s00360-012-0726-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-012-0726-z

Keywords

Search

Navigation