Parasitism of an insect Manduca sexta L. alters feeding behaviour and nutrient utilization to influence developmental success of a parasitoid

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 178, Issue 4, 2008, Pages 515-527

  Thompson, S N ^a   Redak, R A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cotesia congregata; Manduca sexta; Nutrient utilization; Nutrition; Parasitism

Indexed keywords

NITROGEN;

ANIMAL; ANIMAL FOOD; ARTICLE; CARBOHYDRATE DIET; ENERGY METABOLISM; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LARVA; LEPIDOPTERA; LIPID METABOLISM; METABOLISM; PARASITOLOGY; PROTEIN INTAKE; TIME; WASP;

ANIMAL NUTRITION PHYSIOLOGY; ANIMALS; DIETARY CARBOHYDRATES; DIETARY PROTEINS; ENERGY METABOLISM; FEEDING BEHAVIOR; HOST-PARASITE INTERACTIONS; LARVA; LIPID METABOLISM; MANDUCA; NITROGEN; TIME FACTORS; WASPS;

COTESIA CONGREGATA; HEXAPODA; MANDUCA SEXTA;

EID: 42249099831     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-007-0244-6     Document Type: Article

References (62)

1. Adamo S, Shoemaker KL (2000) Effects of parasitism on octopamine content of the central nervous system of Manduca sexta; a possible mechanism underlying host behavioural change. Can J Zool 78:1580-1587
2. Ahmad IM, Waldbauer GP, Friedman S (1989) A defined artificial diet for the larvae of Manduca sexta. Entomol Exp Appl 53:189-192
3. Alleyne M (1995) Alterations in host growth and metabolism of Manduca sexta larvae parasitized by Cotesia congregata, MS Thesis. University of California, Riverside
4. Alleyne M, Beckage NE (1997) Parasitism-induced effects on host growth and metabolic efficiency in tobacco hornworm larvae parasitized by Cotesia congregata. J Insect Physiol 43:407-424
5. Alleyne M, Chappell MA, Beckage NE (1997) Effects of parasitism by the braconid wasp Cotesia congregata on metabolic rate in host larvae of the tobacco hornworm, Manduca sexta. J Insect Physiol 43:143-154
6. Amaya KE, Asgari S, Jung R, Hongskula M, Beckage NE (2005) Parasitization of Manduca sexta larvae bya the parasitoid wasp Cotesia congregata induces an impaired host immune response. J Insect Physiol 51:505-512
7. Askew RR (1971) Parasitic insects. Elsevier, New York
8. Baker FC, Tsai LW, Reuter CC, Schooley DA (1987) In vivo fluctuations of JH, JH acid, and ecdysteroid titer, and JH esterase activity, during development of fifth stadium Manduca sexta. Insect Biochem 17:989-996
9. Beckage NE (1998) Modulation of immune responses to parasitoids by polydnaviruses. Parasitology 116:57-64
10. Beckage NE, Gelman DB (2001) Parasitism of Manduca sexta by Cotesia congregata: a multitude of disruptive endocrine effects. In: Edwards JP, Weaver RJ (eds) Endocrine interactions of insect parasites and pathogens. Biosis Scientific Publishers, Oxford, pp 59-81
11. Bell RA, Joachim RG (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365-373
12. Bede JC, McNeil JN, Tobe SS (2007) The role of neuropeptides in caterpillar nutritional ecology. Peptides 28:185-196
13. Cohen RW, Friedman S, Waldbauer GP (1988) Physiological control of nutrient self-selection in Heliothis zea larvae: the role of serotonin. J Insect Physiol 34:935-940
14. Cohen RW, Mahoney DA, Can HD (2002) Possible regulation of feeding behavior in cockroach nymphs by the neurotransmitter octopamine. J Insect Behav 15:37-50
15. Cole TJ, Beckage NE, Tan FF, Srinivasan A, Ramaswamy SB (2002) Parasitoid-host endocrine relations: self-reliance or co-optation? Insect Biochem Mol Biol 32:1673-1679
16. Combes C (2001) The ecology and evolution of intimate interactions. University of Chicago Press, Chicago
17. Dahlman DL, Green JR (1981) Larval hemolymph protein patterns in tobacco hornworms parasitized by Apanteles congregatus. Ann Entomol Soc Am 74:130-133
18. Dawkins R (1999) Host phenotypes and parasite genes. In: The extended phenotype/the long reach of the gene. Oxford University Press, Oxford, 336pp
19. Edwards JP, Weaver RJ, Marris GC (2001) Endocrine changes in lepidopteran larvae: potential challenges to parasitoid development and survival. In: Edwards JP, Weaver RJ (eds) Endocrine interactions of insect parasites and pathogens. Biosis Scientific Publishers, Oxford, pp 1-32
20. Eggleton P, Gaston KJ (1990) Parasitoid species and assemblages- convenient definitions or misleading compromises. Oikos 59:417-421
21. Eggleton P, Belshaw R (1992) Insect parasitoids: an evolutionary overview. Philos Trans R Soc Lond B 337:1-20
22. Espagne E, Douris V, Lalmanach G, Provost B, Cattolico, Lesobre J, Kurata S, Iatrou K, Drezen J-M, Huguet E (2005) A virus essential for insect host-parasite interactions encodes cystatins. J Virol 79:9765-9776
23. Ewald PW (1995) The evolution of virulence: a unifying link between parasitology and ecology. J Parasitol 81:659-669
24. Federici BA, Bigot Y (2003) Origin and evolution of polydnaviruses by symbiogenesis of insect DNA viruses in endoparasitic wasps. J Insect Physiol 49:419-432
25. Fox GA (2001) Failure-time analysis: studying times to events and rates at which events occur. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 235-266
26. Glendinning JI, Slansky F (1994) Interactions of allelochemicals with dietary constituents: effects on deterrency. Physiol Entomol 19:173-186
27. Hearaty JM (2007) Parasitoid biodiversity and insect pest management. In: Foottit R, Adler P (eds) Insect biodiversity: science and society. Blackwell Scientific, Oxford (in press)
28. Haunerland NH, Shirk PD (1995) Regional and functional differentiation in the insect fat body. Annu Rev Entomol 40:121-145
29. Horton DR, Redak RA (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263-275
30. Jones D, Jones G, Rudnicka M, Click A, Reck-Melleczewen V, Iwaya M (1986) Pseudoparasitism of host Trichoplusia ni by Chelonus spp. as a new model system for parasite regulation of host physiology. J Insect Physiol 32:315-328
31. Keeley LL (1985) Physiology and biochemistry of the fat body. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 3. Permagon, Oxford, pp 211-248
32. Kelly TJ, Gelman DB, Reed DA, Beckage NE (1998) Effects of parasitization by Cotesia congregata on the brain-prothoracic gland axis of its host, Manduca sexta. J Insect Physiol 44:323-332
33. Lee KP, Behmer ST, Simpson SJ, Raubenheimer D (2002) A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). J Insect Physiol 48:655-665
34. Poulin R (1995) Adaptive change in the hehaviour of parasitized animals: a critical review. Int J Parasitol 25:1371-1383
35. Quickie DLJ (1997) Parasitic wasps. Chapman and Hall, London
36. Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomol Exp Appl 62:221-231
37. Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10:151-179
38. Raubenheimer D, Simpson SJ (1999) Integrating nutrition: a geometrical approach. Entomol Exp Appl 91:67-82
39. Raubenheimer D, Simpson SJ (2003) Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. J Exp Biol 206:1669-1681
40. Roberts LS, Janovy J Jr (2005) Gerald D Schmidt and Larry S Roberts, Foundations of parasitology, 7th edn. McGraw-Hill, Boston
41. Rogers SM, Matheson T, Sasaki K, Kendrick K, Simpson SJ, Burrows M. (2004) Substantial changes in central nervous system neurotransmitters and neruomodulators accompany phase change in the locust. J Exp Biol 207:3603-3617
42. Simpson SJ, Raubenheimer D (1993a) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc 342:381-402
43. Simpson SJ, Raubenheimer D (1993b) The central role of haemolymph in the regulation of nutrient intake in insects. Physiol Entomol 18:395-403
44. Simpson SJ, Raubenheimer D (1996) Feeding behaviour, sensory physiology and nutritional feedback: an integrative model. Entomol Exp App 80:55-64
45. Simpson SJ, White P (1990) Associative learning and locust feeding: evidence for a "learned hunger" for protein. Anim Behav 40:506-513
46. Singer MS, Carriere Y, Theuring C, Hartmann T (2004) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Amer Nat 164: 423-429
47. Slansky F Jr (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. J Insect Physiol 32:255-261
48. Slansky F (1992) Allelochemical-nutrient interactions in herbivore nutritional ecology. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 135-174
49. Slansky F Jr, Scriber JM (1985) Food consumption and utilization. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 4. Permagon, Oxford, pp 87-163
50. Thompson SN (1990) Physiological alterations during parasitism and their effects on host behaviour. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor and Francis, London, pp 64-94
51. Thompson SN (1999) Nutrition of entomophagous insects and other arthropods. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, New York, pp 594-652
52. Thompson SN (1993) Redirection of host metabolism and effects on parasite nutrition. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects, vol 1. Academic Press, New York, pp 125-144
53. Thompson SN (2001) Parasitism enhances the induction of glucogenesis by the insect, Manduca sexta L. Int J Biochem Cell Biol 33:163-173
54. Thompson SN, Redak RA (2005) Feeding behaviour and nutrient selection in an insect Manduca sexta L. and alterations induced by parasitism. J Comp Physiol A 191:909-923
55. Thompson SN, Redak RA (2007) Nicotine moderates the effects of macronutrient balance on nutrient intake by parasitized Manduca sexta L. J Comp Physiol B 177:375-391
56. Thompson SN, Borchardt DB, Wang L-W (2003) Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. J Comp Physiol B 173:149-163
57. Thompson SN, Redak RA, Borchardt DB (2002) The glucogenic response of a parasitized insect Manduca sexta L. is partially mediated by differential nutrient intake. Biochim Biophys Acta 1571:138-150
58. Thompson SN, Redak RA, Wang L-W (2001) Altered dietary nutrient intake maintains metabolic homeostasis in parasitized larvae of the insect Manduca sexta L. J Exp Biol 204:4065-4080
59. Thompson SN, Redak RA, Wang L-W (2005a) Nutrition interacts with parasitism to influence growth and physiology of the insect Manduca sexta L. J Exp Biol 208:611-623
60. Thompson SN, Redak RA, Wang L-W (2005b) Host nutrition determines blood nutrient composition and mediates parasite developmental success: Manduca sexta L. parasitized by Cotesia congregata (Say). J Exp Biol 208:625-635
61. Zanotto FP, Simpson SJ, Raubenheimer D (1993) The regulation of growth by locusts through post-ingestive compensation for variation in the levels of protein and carbohydrate. Physiol Entomol 18:425-434
62. Zanotto FP, Gouveia SM, Simpson SJ, Raubenheimer D, Calder PC (1997) Nutritional homeostasis in locusts: is there a mechanism for increased energy expenditure during carbohydrate overfeeding? J Exp Biol 200:2437-2448