Skip to main content
Log in

Separate effects of macronutrient concentration and balance on plastic gut responses in locusts

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

Abstract

It is well established that animal guts are phenotypically plastic, adjusting inter-alia to diet quality. However, the relative contributions due to the two principal dimensions of diet “quality”—nutrient concentration and nutrient balance—remain to be teased apart. We report an experiment using synthetic foods in which the balance and overall concentration (in relation to indigestible cellulose) of protein and digestible carbohydrate were varied orthogonally, and the effects on the dry mass of locust guts measured. There were three principal results: (1) larger guts were associated with dilute compared with concentrated diets, suggesting a compensatory response to ameliorate the impact of reduced diet quality; (2) there was, by contrast, an anti-compensatory response to nutrient imbalance, where larger guts were associated with surplus protein intake; (3) the experimental group given the food that contained low protein and low cellulose, the composition that predicted the smallest guts, showed a bimodal response in which half of the insects had guts that were larger than expected for their cellulose intake, suggesting that they were able to respond to a protein-related cue in the absence of significant dietary fibre. We discuss these results in relation to regulatory theory.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Battley PF, Piersma T (2005) Adaptive interplay between feeding ecology and features of the digestive tract in birds. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 201–227

    Google Scholar 

  • Bines JE, Taylor RG, Justice F, Paris MCJ, Sourial M, Nagy E, Emselle S, Catto-Smith AG, Fuller PJ (2002) Influence of diet complexity on intestinal adaptation following massive small bowel resection in a preclinical model. J Gastroenterol Hepatol 17:1170–1179

    Article  PubMed  CAS  Google Scholar 

  • Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330

    Article  PubMed  Google Scholar 

  • Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  PubMed  Google Scholar 

  • Buddington RK (1987) Does the natural diet influence the intestines ability to regulate glucose-absorption?. J Comp Physiol [B] 157:677–688

    CAS  Google Scholar 

  • Chapman RF (1988) Variations in the size of the midgut caeca during the fifth instar of the grasshopper, Schistocerca americana (Drury). J Insect Physiol 34:329–335

    Article  Google Scholar 

  • Conover WJ, Iman RL (1982) Analysis of covariance using the rank transformation. Biometrics 38:715–724

    Article  PubMed  CAS  Google Scholar 

  • Dadd RH (1961) The nutritional requirements of locusts IV. Requirements for vitamins of the b-complex. J Insect Physiol 6:1–12

    Article  CAS  Google Scholar 

  • Delorme CB, Wojcik J, Gordon C (1981) Method of addition of cellulose to experimental diets and its effect on rat growth and protein-utilization. J Nutr 111:1522–1527

    PubMed  CAS  Google Scholar 

  • Diamond JM, Hammond K (1992) The matches, achieved by natural selection, between biological capacities and their natural loads. Experientia 48:551–557

    Article  PubMed  CAS  Google Scholar 

  • Dow JAT (1986) Insect midgut function. Adv Insect Physiol 19:187–328

    Article  CAS  Google Scholar 

  • Elsenhans B, Caspary WF (2000) Food viscosity as determinant for adaptive growth responses in rat intestine: long-term feeding of different hydroxyethyl celluloses. Br J Nutr 84:39–48

    PubMed  CAS  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, Solberg DH, Diamond JM (1987) Dependence of intestinal amino acid uptake on dietary protein or amino acid levels. Am J Physiol Gastrointest Liver Physiol 252:G614–G625

    CAS  Google Scholar 

  • Lee K-P, Raubenheimer D, Simpson SJ (2004) The effects of nutritional imbalance on compensatory feeding for cellulose-mediated dietary dilution in a generalist caterpillar. Physiol Entomol 29:108–117

    Article  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 adaptive behaviour. Trends Ecol Evol 12:134–138

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10:151–179

    Article  CAS  PubMed  Google Scholar 

  • Raubenheimer D, Simpson SJ (1998) Nutrient transfer functions: the site of integration between feeding behaviour and nutritional physiology. Chemoecology 8:61–68

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ (2003) Nutrient balancing in grasshoppers: Behavioural and physiological correlates of dietary breadth. J Exp Biol 206:1669–1681

    Article  PubMed  CAS  Google Scholar 

  • Raubenheimer D, Lee K-P, Simpson SJ (2005) Does Bertrand’s rule apply to macronutrients? Proc Biol Sci 272:2429–2434

    Article  PubMed  CAS  Google Scholar 

  • Seaman JW, Walls SC, Wise SE, Jaeger RG (1994) Caveat emptor: rank transform methods and interaction. Trends Ecol Evol 9:261–263

    Article  Google Scholar 

  • Secor SM, Whang EE, Lane JS, Ashley SW, Diamond J (2000) Luminal and systemic signals trigger intestinal adaptation in the juvenile python. Am J Physiol Gastrointest Liver Physiol 279:G1177–G1187

    PubMed  CAS  Google Scholar 

  • Secor SM, Lane JS, Whang EE, Ashley SW, Diamond J (2002) Luminal nutrient signals for intestinal adaptation in pythons. Am J Physiol Gastrointest Liver Physiol 283:G1298–G1309

    PubMed  CAS  Google Scholar 

  • Sibly RM (1981) Strategies of digestion and defecation, chap 5. In: Townsend CR, Calow P (eds) Physiological ecology: an evolutionary approach. Blackwell, Oxford, pp 109–139

    Google Scholar 

  • Simpson SJ, Abisgold JD (1985) Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Physiol Entomol 10:443–452

    Google Scholar 

  • Simpson SJ, Raubenheimer D (1993) The central role of the haemolymph in the regulation of nutrient intake in insects. Physiol Entomol 18:395–403

    Article  CAS  Google Scholar 

  • Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311

    Article  Google Scholar 

  • Spector MH, Levine GM, Deren JJ (1977) Direct and indirect effects of dextrose and amino-acids on gut mass. Gastroenterology 72:706–710

    PubMed  CAS  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 

  • Yang Y, Joern A (1994) Gut size changes in relation to variable food quality and body size in grasshoppers. Funct Ecol 8:36–45

    Article  Google Scholar 

  • Zanotto FP, Simpson SJ, Raubenheimer D (1993) The regulation of growth by locusts through post-ingestive compensation for variation in the levels of dietary protein and carbohydrate. Physiol Entomol 18:425–434

    Article  Google Scholar 

Download references

Acknowledgments

We thank Professor Steve Simpson and Dr David Mayntz for commenting on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Raubenheimer.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raubenheimer, D., Bassil, K. Separate effects of macronutrient concentration and balance on plastic gut responses in locusts. J Comp Physiol B 177, 849–855 (2007). https://doi.org/10.1007/s00360-007-0180-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-007-0180-5

Keywords

Navigation