The Science of Nature

, 102:40 | Cite as

Food restriction alters energy allocation strategy during growth in tobacco hornworms (Manduca sexta larvae)

  • Lihong Jiao
  • Kaushalya Amunugama
  • Matthew B. Hayes
  • Michael Jennings
  • Azriel Domingo
  • Chen Hou
Original Paper


Growing animals must alter their energy budget in the face of environmental changes and prioritize the energy allocation to metabolism for life-sustaining requirements and energy deposition in new biomass growth. We hypothesize that when food availability is low, larvae of holometabolic insects with a short development stage (relative to the low food availability period) prioritize biomass growth at the expense of metabolism. Driven by this hypothesis, we develop a simple theoretical model, based on conservation of energy and allometric scaling laws, for understanding the dynamic energy budget of growing larvae under food restriction. We test the hypothesis by manipulative experiments on fifth instar hornworms at three temperatures. At each temperature, food restriction increases the scaling power of growth rate but decreases that of metabolic rate, as predicted by the hypothesis. During the fifth instar, the energy budgets of larvae change dynamically. The free-feeding larvae slightly decrease the energy allocated to growth as body mass increases and increase the energy allocated to life sustaining. The opposite trends were observed in food restricted larvae, indicating the predicted prioritization in the energy budget under food restriction. We compare the energy budgets of a few endothermic and ectothermic species and discuss how different life histories lead to the differences in the energy budgets under food restriction.


Food restriction Energy budget Scaling law Growth Manduca sexta 



We gratefully acknowledge the careful reviews and suggestions of three anonymous reviewers. We would like to thank Dr. Rex Gerald for his help with measuring combustion energy content of larval tissue and feces, Dr. Toomas Tammaru and Dr. Douglas Glazier for their excellent suggestions that helped to develop the hypothesis, and Dr. Wenyun Zuo for her enlightening discussion.

Supplementary material

114_2015_1289_MOESM1_ESM.docx (172 kb)
ESM 1 (DOCX 172 kb)


  1. Benyi K, Habi H (1998) Effects of food restriction during the finishing period on the performance of broiler chickens. Br Poult Sci 39:423–425CrossRefPubMedGoogle Scholar
  2. Bernays EA, Woods HA (2000) Foraging in nature by larvae of < i > Manduca sexta</i > —influenced by an endogenous oscillation. J Insect Physiol 46:825–836CrossRefPubMedGoogle Scholar
  3. Brody S (1945) Bioenergetics and growth. Reinhold, New YorkGoogle Scholar
  4. Campero M, De Block M, Ollevier F, Stoks R (2008) Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality. Funct Ecol 22:271–277CrossRefGoogle Scholar
  5. D’Amico LJ, Davidowitz G, Nijhout HF (2001) The developmental and physiological basis of body size evolution in an insect. Proc R Soc Lond B Biol Sci 268:1589–1593. doi: 10.1098/rspb.2001.1698 CrossRefGoogle Scholar
  6. Davidowitz G, D’Amico LJ, Nijhout HF (2003) Critical weight in the development of insect body size. Evol Dev 5:188–197. doi: 10.1046/j.1525-142X.2003.03026.x CrossRefPubMedGoogle Scholar
  7. De Block M, Stoks R (2008) Short-term larval food stress and associated compensatory growth reduce adult immune function in a damselfly. Ecol Entomol 33:796–801. doi: 10.1111/j.1365-2311.2008.01024.x CrossRefGoogle Scholar
  8. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116. doi: 10.1111/j.1469-185X.2010.00136.x CrossRefPubMedGoogle Scholar
  9. Esperk T, Tammaru T (2004) Does the ‘investment principle’model explain moulting strategies in lepidopteran larvae? Physiol Entomol 29:56–66CrossRefGoogle Scholar
  10. Glazier DS (2002) Resource-allocation rules and the heritability of traits. Evolution 56:1696–1700. doi: 10.1111/j.0014-3820.2002.tb01481.x CrossRefPubMedGoogle Scholar
  11. Glazier DS (2005) Beyond the “3/4 power law”: variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev 80:611. doi: 10.1017/s1464793105006834 CrossRefPubMedGoogle Scholar
  12. Glazier DS, Calow P (1992) Energy allocation rules in Daphnia magna: clonal and age differences in the effects of food limitation. Oecologia 90:540–549CrossRefGoogle Scholar
  13. Greenlee KJ, Harrison JF (2005) Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar. Manduca sexta J Exp Biol 208:1385–1392. doi: 10.1242/jeb.01521 CrossRefPubMedGoogle Scholar
  14. Grodzinski W, Klekowski RZ, Duncan A (1975) Methods for ecological bioenergetics. Blackwell Scientific Publications, OxfordGoogle Scholar
  15. Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56:103–121. doi: 10.1146/annurev-ento-112408-085436 CrossRefPubMedGoogle Scholar
  16. Hayes SE, McClintock JB, Watson CJ, Douglas Watson R (1992) Growth, energetics and food conversion efficiency during the last larval stadium of the tobacco hornworm (Manduca sexta). Comp Biochem Physiol A Physiol 102:395–399. doi: 10.1016/0300-9629(92)90153-h CrossRefGoogle Scholar
  17. Hayes M, Jiao L, Tsao T-h, King I, Jennings M, Hou C (2014) High temperature slows down growth in tobacco hornworms (Manduca sexta larvae) under food restriction Insect Sci In press doi: 10.1111/1744-7917.12109
  18. Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship Oikos:483–492Google Scholar
  19. Hou C (2013) The energy trade-off between growth and longevity. Mech Ageing Dev 134:373–380. doi: 10.1016/j.mad.2013.07.001 CrossRefPubMedGoogle Scholar
  20. Hou C (2014) Increasing energetic cost of biosynthesis during growth makes refeeding deleterious. Am Nat 184:233–247. doi: 10.1086/676856 CrossRefPubMedGoogle Scholar
  21. Hou C, Zuo WY, Moses ME, Woodruff WH, Brown JH, West GB (2008) Energy uptake and allocation during ontogeny. Science 322:736–739. doi: 10.1126/science.1162302 PubMedCentralCrossRefPubMedGoogle Scholar
  22. Hou C, Bolt KM, Bergman A (2011a) Energetic basis of correlation between catch-up growth. health maintenance, and aging. J Gerontol A Biol Sci Med Sci 66A:627–638. doi: 10.1093/gerona/glr027 PubMedCentralCrossRefGoogle Scholar
  23. Hou C, Bolt KM, Bergman A (2011b) A general model for ontogenetic growth under food restriction. Proc R Soc B Biol Sci 278:2881–2890. doi: 10.1098/rspb.2011.0047 CrossRefGoogle Scholar
  24. Jokela J (1997) Optimal energy allocation tactics and indeterminate growth: life-history evolution of long-lived bivalves. In: Evolutionary Ecology of Freshwater Animals. Springer, pp 179–196Google Scholar
  25. Kearney MR, White CR (2012) Testing metabolic theories. Am Nat 180:546CrossRefPubMedGoogle Scholar
  26. Kingsolver JG, Woods HA (1997) Thermal sensitivity of growth and feeding in Manduca sexta caterpillars. Physiol Biochem Zool 70:631–638Google Scholar
  27. Kitaysky AS (1999) Metabolic and developmental responses of alcid chicks to experimental variation in food intake. Physiol Biochem Zool 72:462–473CrossRefPubMedGoogle Scholar
  28. Konarzewski M, Starck JM (2000) Effects of food shortage and oversupply on energy utilization, histology, and function of the gut in nestling song thrushes (Turdus philomelos). Physiol Biochem Zool 73:416–427CrossRefPubMedGoogle Scholar
  29. Kooijman S (2010) Dynamic energy budget theory. Cambridge University Press, CambridgeGoogle Scholar
  30. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, USACrossRefGoogle Scholar
  31. Maltby L (1994) Stress, shredders and streams: using Gammarus energetics to assess water qualityGoogle Scholar
  32. Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176. doi: 10.1086/444439 CrossRefPubMedGoogle Scholar
  33. Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583–593Google Scholar
  34. McCarter RJ, Palmer J (1992) Energy-metabolism and aging—a lifelong study of Fischer-344 rats. Am J Physiol-Endocrinol Metab 263:E448–E452Google Scholar
  35. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  36. Morgan IJ, Metcalfe NB (2001) Deferred costs of compensatory growth after autumnal food shortage in juvenile salmon. Proc R Soc Lond B Biol Sci 268:295–301. doi: 10.1098/rspb.2000.1365 CrossRefGoogle Scholar
  37. Naim M, Brand JG, Kare MR, Kaufmann NA, Kratz CM (1980) Effects of unpalatable diets and food restriction on feed efficiency in growing rats. Physiol Behav 25:609–614. doi: 10.1016/0031-9384(80)90360-1 CrossRefPubMedGoogle Scholar
  38. Nijhout HF (1975) A threshold size for metamorphosis in the tobacco hornworm. Manduca sexta (L) Biol Bull 149:214–225CrossRefPubMedGoogle Scholar
  39. Nijhout H, Davidowitz G, Roff D (2006) A quantitative analysis of the mechanism that controls body size in Manduca sexta. J Biol 5:16PubMedCentralCrossRefPubMedGoogle Scholar
  40. Ocak N, Erener G (2005) The effects of restricted feeding and feed form on growth, carcass characteristics and days to first egg of Japanese quail (Coturnix coturnix japonica). Asian Austral J Anim Sci 18:1479CrossRefGoogle Scholar
  41. Pietrzak B, Grzesiuk M, Bednarska A (2010) Food quantity shapes life history and survival strategies in Daphnia magna (Cladocera). Hydrobiologia 643:51–54CrossRefGoogle Scholar
  42. Reynolds SE, Nottingham SF (1985) Effects of temperature on growth and efficiency of food utilization in fifth-instar caterpillars of the tobacco hornworm, Manduca sexta. J Insect Physiol 31:129–134. doi: 10.1016/0022-1910(85)90017-4 CrossRefGoogle Scholar
  43. Roff DA (2001) Life history evolution. Sinauer Associates, SunderlandGoogle Scholar
  44. Rønning B, Mortensen AS, Moe B, Chastel O, Arukwe A, Bech C (2009) Food restriction in young Japanese quails: effects on growth, metabolism, plasma thyroid hormones and mRNA species in the thyroid hormone signalling pathway. J Exp Biol 212:3060–3067. doi: 10.1242/jeb.029835 CrossRefPubMedGoogle Scholar
  45. Sears KE, Kerkhoff AJ, Messerman A, Itagaki H (2012) Ontogenetic Scaling of metabolism, growth, and assimilation: testing metabolic scaling theory with manduca sexta larvae. Physiol Biochem Zool 85:159–173CrossRefPubMedGoogle Scholar
  46. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  47. Steinberg CE, Ouerghemmi N, Herrmann S, Bouchnak R, Timofeyev MA, Menzel R (2010) Stress by poor food quality and exposure to humic substances: Daphnia magna responds with oxidative stress, lifespan extension, but reduced offspring numbers. Hydrobiologia 652:223–236CrossRefGoogle Scholar
  48. Timmins WA, Bellward K, Stamp AJ, Reynolds SE (1988) Food intake, conversion efficiency, and feeding behaviour of tobacco hornworm caterpillars given artificial diet of varying nutrient and water content. Physiol Entomol 13:303–314. doi: 10.1111/j.1365-3032.1988.tb00482.x CrossRefGoogle Scholar
  49. West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592. doi: 10.1242/jeb.01589 CrossRefPubMedGoogle Scholar
  50. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126CrossRefPubMedGoogle Scholar
  51. Withers PC (1992) Comparative animal physiology. Saunders College Pub, Fort WorthGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Lihong Jiao
    • 1
  • Kaushalya Amunugama
    • 1
  • Matthew B. Hayes
    • 1
  • Michael Jennings
    • 1
  • Azriel Domingo
    • 1
  • Chen Hou
    • 1
  1. 1.Department of Biological ScienceMissouri University of Science and TechnologyRollaUSA

Personalised recommendations