Caterpillars use developmental plasticity and diet choice to overcome the early life experience of nutritional imbalance

Animal Behaviour

Volumn 84, Issue 4, 2012, Pages 785-793

  Lee, Kwang Pum ^a,b   Kwon, Soon Tak ^a   Roh, Chris ^a  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Compensation; Developmental plasticity; Diet choice; Foraging behaviour; Herbivory; Nutrient balancing; Protein:carbohydrate balance; Spodoptera litura

Indexed keywords

BIOLOGICAL UPTAKE; CARBOHYDRATE; CATERPILLAR; COMPENSATION; DEVELOPMENTAL BIOLOGY; DIET; FITNESS; FORAGING BEHAVIOR; HETEROGENEITY; NUTRITIONAL STATUS; PHENOTYPIC PLASTICITY; PLANT-HERBIVORE INTERACTION; PROTEIN;

SPODOPTERA LITURA;

EID: 84866907925     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2012.06.033     Document Type: Article

References (64)

1. Barata C., Baird D.J., Soares A.M. Phenotypic plasticity in Daphnia magna Straus: variable maturation instar as an adaptive response to predation pressure. Oecologia 2001, 129:220-227.
2. Barrett E.L.B., Hunt J., Moore A.J., Moore P.J. Separate and combined effects of nutrition during juvenile and sexual development on female life history trajectories: the thrifty phenotype in a cockroach. Proceedings of the Royal Society B 2009, 276:3257-3264.
3. Barton Browne L. Ontogenic changes in feeding behavior. Regulatory Mechanism in Insect Feeding 1995, 307-342. Chapman & Hall, New York. R.F. Chapman, G. de Boer (Eds.).
4. Behmer S.T. Insect herbivore nutrient regulation. Annual Review of Entomology 2009, 54:165-187.
5. Benrey B., Denno R.F. The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 1997, 78:987-999.
6. Bernays E.A., Chapman R.F. Host-Plant Selection by Phytophagous Insects 1994, Chapman & Hall, New York.
7. Boggs C.L., Freeman K.D. Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 2005, 144:353-361.
8. Brown E.S., Dewhurst C.F. The genus Spodoptera in Africa and the Near East. Bulletin of Entomological Research 1975, 65:221-262.
9. Cook R.T., Bailey S.E.R., McCrohan C.R., Nash B., Woodhouse R.M. The influence of nutritional status on the feeding behaviour of the field slug, Deroceras reticulatum (Müller). Animal Behaviour 2000, 59:167-176.
10. Clissold F.J., Tedder B.J., Conigrave A.D., Simpson S.J. The gastrointestinal tract as a nutrient-balancing organ. Proceedings of the Royal Society B 2010, 277:1751-1759.
11. Crawley M.J. The R Book 2007, J. Wiley, New York.
12. Diamond S.E., Kingsolver J.G. Environmental dependence of thermal reaction norms: host plant quality can reverse the temperature-size rule. American Naturalist 2010, 175:1-10.
13. Dmitriew C., Rowe L. Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis). Journal of Evolutionary Biology 2007, 20:1298-1310.
14. Dmitriew C., Rowe L. The effects of larval nutrition on reproductive performance in a food-limited adult environment. PloS One 2011, 6:e17399.
15. Esperk T., Tammaru T., Nylin S. Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology 2007, 100:627-645.
16. Fox G.A. Failure-time analysis: emergence, flowering, survivorship, and other waiting times. Design and Analysis of Ecological Experiments 2001, 235-266. Oxford University Press, Oxford. 2nd edn. S.M. Scheiner, J. Gurevitch (Eds.).
17. Higgins L.E., Rankin M.A. Different pathways in arthropod postembryonic development. Evolution 1996, 50:573-582.
18. Honek A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 1993, 66:483-492.
19. Houston A.I., Higginson A.D., McNamara J.M. Optimal foraging for multiple nutrients in an unpredictable environment. Ecology Letters 2011, 14:1101-1107.
20. Jensen K., Mayntz D., Toft S., Clissold F.J., Hunt J., Raubenheimer D., Simpson S.J. Optimal foraging for specific nutrients in predatory beetles. Proceedings of the Royal Society B 2012, 279:2212-2218.
21. Kingsolver J.G. Variation in growth and instar number in field and laboratory Manduca sexta. Proceedings of the Royal Society B 2007, 274:977-981.
22. Lee K.P. Sex-specific differences in nutrient regulation in a capital breeding caterpillar, Spodoptera litura (Fabricius). Journal of Insect Physiology 2010, 56:1685-1695.
23. Lee K.P., Behmer S.T., Simpson S.J., Raubenheimer D. A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology 2002, 48:655-665.
24. Lee K.P., Raubenheimer D., Behmer S.T., Simpson S.J. A correlation between macronutrient balancing and insect host-plant range: evidence from the specialist caterpillar Spodoptera exempta (Walker). Journal of Insect Physiology 2003, 49:1161-1171.
25. Lee K.P., Simpson S.J., Clissold F.J., Brooks R., Ballard J.W.O., Taylor P.W., Soran N., Raubenheimer D. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Sciences, U.S.A. 2008, 105:2498-2503.
26. Littell R.C., Miliken G.A., Stroup W.W., Wolfinger R.D., Schabenberger O. SAS for Mixed Models 1996, SAS Institute Inc, Cary, North Carolina. 2nd edn.
27. Loader C., Damman H. Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 1991, 72:1586-1590.
28. McNamara J.M., Houston A.I. Starvation and predation as factors limiting population size. Ecology 1987, 68:1515-1519.
29. Mayntz D., Raubenheimer D., Salomon M., Toft S., Simpson S.J. Nutrient-specific foraging in invertebrate predators. Science 2005, 307:111-113.
30. Metcalfe N.B., Monaghan P. Compensation for a bad start: grow now, pay later?. Trends in Ecology and Evolution 2001, 16:254-260.
31. Mevi-Schütz J., Erhardt A. Amino acids in nectar enhance butterfly fecundity: a long-awaited link. American Naturalist 2005, 165:411-419.
32. Monaghan P. Early growth conditions, phenotypic development and environmental change. Philosophical Transactions of the Royal Society B 2008, 363:1635-1643.
33. Morita M., Tojo S. Relationship between starvation and supernumerary ecdysis and recognition of the penultimate-larval instar in the common cutworm, Spodoptera litura. Journal of Insect Physiology 1985, 31:307-313.
34. Nijhout H.F. A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta. Biological Bulletin 1975, 149:214-225.
35. Nijhout H.F. Insect Hormones 1994, Princeton University Press, Princeton, New Jersey.
36. Nylin S., Gotthard K. Plasticity in life history traits. Annual Review of Entomology 1998, 43:63-83.
37. Raubenheimer D., Jones S.A. Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Animal Behaviour 2006, 71:1253-1262.
38. Raubenheimer D., Simpson S.J. Analysis of covariance: an alternative to nutritional indices. Entomologia Experimentalis et Applicata 1992, 62:221-231.
39. Raubenheimer D., Simpson S.J. The analysis of nutrient budgets. Functional Ecology 1994, 8:783-791.
40. Raubenheimer D., Simpson S.J. Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. Journal of Experimental Biology 2003, 206:1669-1681.
41. Raubenheimer D., Lee K.P., Simpson S.J. Does Bertrand's rule apply to macronutrients?. Proceedings of the Royal Society B 2005, 272:2429-2434.
42. Raubenheimer D., Simpson S.J., Mayntz D. Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology 2009, 23:4-16.
43. Reavey D. Why body size matters to caterpillars. Caterpillars: Ecological and Evolutionary Constraints on Foraging 1993, 248-279. Chapman & Hall, New York. N.E. Stamp, T.M. Casey (Eds.).
44. Roff D.A. The Evolution of Life Histories: Theory and Analysis 1992, Chapman & Hall, New York.
45. Scheiner S.M. MANOVA: multiple response variables and multispecies interactions. Design and Analysis of Ecological Experiments 2001, 99-115. Oxford University Press, Oxford. 2nd edn. S.M. Scheiner, J. Gurevitch (Eds.).
46. Simmonds M.S.J., Simpson S.J., Blaney W.M. Dietary selection behaviour in Spodoptera littoralis: the effects of conditioning diet and conditioning period on neural responsiveness and selection behaviour. Journal of Experimental Biology 1992, 162:73-90.
47. Simpson S.J., Abisgold J.D. Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Physiological Entomology 1985, 10:443-452.
48. Simpson S.J., Raubenheimer D. A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philosophical Transactions of the Royal Society B 1993, 342:381-402.
49. Simpson S.J., Raubenheimer D. The central role of the haemolymph in the regulation of nutrient intake in insects. Physiological Entomology 1993, 18:395-403.
50. Simpson S.J., White P. Associative learning and locust feeding: evidence for a 'learned hunger' for protein. Animal Behaviour 1990, 40:506-513.
51. Simpson S.J., Simmonds M.S.J., Blaney W.M. A comparison of dietary selection behaviour in larval Locusta migratoria and Spodoptera littoralis. Physiological Entomology 1988, 13:225-238.
52. Simpson S.J., Simmonds M.S.J., Blaney W.M., Jone J.P. Compensatory dietary selection occurs in larval Locusta migratoria but not Spodoptera littoralis after a single deficient meal during ad libitum feeding. Physiological Entomology 1990, 15:235-242.
53. Simpson S.J., Sibly R.M., Lee K.P., Behmer S.T., Raubenheimer D. Optimal foraging when regulating intake of multiple nutrients. Animal Behaviour 2004, 68:1299-1311.
54. Singer M.S., Bernays E.A., Carrière Y. The interplay between nutrient balancing and toxin dilution in foraging by a generalist herbivore. Animal Behaviour 2002, 64:629-645.
55. Stamp N.E., Casey T.M. Caterpillars: Ecological and Evolutionary Constraints on Foraging 1993, Chapman & Hall, New York.
56. Stockhoff B.A. Starvation resistance of gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae): tradeoffs among growth, body size, and survival. Oecologia 1991, 88:422-429.
57. Stockhoff B.A. Diet-switching by gypsy moth: effects of diet nitrogen history versus switching on growth, consumption, and food utilization. Entomologia Experimentalis et Applicata 1992, 64:225-238.
58. Stockhoff B.A. Ontogenetic change in dietary selection for protein and lipid by gypsy moth larvae. Journal of Insect Physiology 1993, 39:677-686.
59. Stoks R., De Block M., McPeek M.A. Physiological costs of compensatory growth in a damselfly. Ecology 2006, 87:1566-1574.
60. Taborsky B. The influence of juvenile and adult environments on life history trajectories. Proceedings of the Royal Society B 2006, 273:741-750.
61. Tammaru T., Nylin S., Ruohomaki K., Gotthard K. Compensatory responses in lepidopteran larvae: a test of growth rate maximization. Oikos 2004, 107:352-362.
62. Taylor M.F.J. Compensation for variable dietary nitrogen by larvae of the salvinia moth. Functional Ecology 1989, 3:407-416.
63. Thompson S.N., Redak R.A. Interactions of dietary protein and carbohydrate determine blood sugar level and regulate nutrient selection in the insect Manduca sexta L. Biochimica et Biophysica Acta 2000, 1523:91-102.
64. Woods H.A. Patterns and mechanisms of growth of fifth-instar Manduca sexta caterpillars following exposure to low- or high-protein food during early instars. Physiological and Biochemical Zoology 1999, 72:445-454.