Abstract
Manduca sexta L. larvae exhibit broad food acceptance with regard to nutrient content during the first 3 days of the last stadium. Larvae fed diets with a constant combined level of casein and sucrose, but variable ratios, display a linear relationship between protein and carbohydrate intake. Larvae grow best on a diet with equal nutrients, but will consume an excess of one nutrient in order to obtain an adequate amount of the other, as nutrient ratio shifts. Parasitized larvae feed similarly, but the nutrient ratio does not affect growth. Unparasitized larvae regulate intake of protein and carbohydrate when offered choices of protein-biased and carbohydrate-biased diets having combined nutrient levels of 120 g/l, but with variable ratios. Larvae normally consume equal amounts of nutrients, regardless of ratio, and grow similarly. As combined nutrient level is reduced in one diet, larvae abandon regulation and feed randomly. Parasitized larvae offered choice diets with 120 g/l combined nutrients do not regulate nutrient intake. Consumption of nutrients varies widely, but growth is unaffected. Larvae offered choices of diets having equal amounts of casein and sucrose but variable fat (corn oil), fail to regulate fat intake, although both unparasitized and parasitized larvae prefer a diet containing higher fat.
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Abbreviations
- ANCOVA :
-
Analysis of covariance
- ANOVA :
-
Analysis of variance
- MANCOVA :
-
Multiple analysis of covariance
- C :
-
Casein
- S :
-
Sucrose
References
Ahmad IM, Waldbauer GP, Friedman S (1989) A defined artifiical diet for the larvae of Manduca sexta. Entomol Exp Appl 53:189–192
Akehurst BC (1981) Tobacco. Longman, New York, pp 522–577
Alleyne M (1995) Alterations in host growth and metabolism of Manduca sexta larvae parasitized by Cotesia congregata. MS Thesis, University of California, Riverside
Bacon CW, Wenger R, Bullock JF (1952) Chemical changes in tobacco during flue-curing. Ind Engng Chem Ind Edn 44:292–296
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
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. BIOS Scientific, Oxford, pp 59–81
Beckage NE, Foreman RC, Palmatier CM, Tan FF (2002) Inhibition of the larval ecdysis and emergence behavior of the parasiitoid Cotesia congregata by methoprene. J Insect Physiol 48:725–732
Bell RA, Joachim RG (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373
Bernays EA (1998) Evolution of feeding behavior in insect herbivores. Success seen as different ways to eat without being eaten. Bioscience 48:35–44
Bernays EA (1999) Plasticity and the problem of choice in food selection. Ann Entomol Soc Am 92:944–951
Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–727
Bernays EA, Chapman RF (1994) Host plant selection by phytophagous insects. Chapman and Hall, New York
Bernays EA, Woods HA (2000) Foraging in nature by larvae of Manduca sexta—influenced by an endogenous oscillation. J Insect Physiol 46:825–836
Bush LP (1999) Alkaloid biosynthesis. In: Davis DL, Nielsen MT (eds) Tobacco production, chemistry and technology. Blackwell, London, pp 285–291
Cohen RW, Friedman S, Waldbauer FP (1998) Physiological control of nutrient self-selection in Heliothis zea larvae: the role of serotonin. J Insect Physiol 34:935–940
del Campo ML, Miles CI (2003) Chemosensory tuning to a host recognition cue in the facultative specialist larvae of the moth Manduca sexta. J Exp Biol 206:3979–3990
del Campo ML, Miles CI, Schroeder FC, Mueller C, Booker R, Renwick JA (2001) Host recognition by the tobacco hornworm is mediated by a host plant compound. Nature 411:186–188
Ehrlich PR, Murphy DD (1988) Plant chemistry and host range in insect herbivores. Ecology 69:910–911
Fernstrom JD (1990) Aromatic amino acids and monoamine synthesis in the central nervous system: influence of the diet. J Nutr Biochem 1:508–517
Fernstrom JD, Fernstrom MH (2001) Monoamines and protein intake: are control mechanisms designed to monitor a threshold intake or a set point?. Nutr Rev 59:S60–S68
von Fircks Y, Ericsson T, Sennerby-Forsse L (2001) Seasonal variation of macronutrients in leaves, stems and roots of Salix dasyclados Wimm. grown at two nutrient levels. Biomass Bioenergy 21:321–334
Gilbert LI, Granger NA, Roe RM (2000) The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem Molec Biol 30:617–644
Glendinning JL (1996) Is chemosensory input essential for the rapid rejection of toxic foods?. J Exp Biol 199:1523–1534
Glendinning JL, Nelson NM, Bernays EA (2000) How do inositol and glucose modulate feeding in Manduca sexta caterpillars?. J Exp Biol 203:1299–1315
Granger NA, Ebersohl R, Sparks TC (2000) Pharmacological characterization of dopamine receptors in the corpus allatum of Manduca sexta larvae. Insect Biochem Molec Biol 30:755–766
Gusewell S, Koerselman M (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Persp Plant Ecol Evol Syst 5:37–61
Hayakawa Y, Noguchi H (1998) Growth-blocking peptide expressed in the insect nervous system. Cloning and functional characterization. Eur J Biochem 252:810–816
Hopkins TL, Starkey SR, Beckage NE (1998) Tyrosine and catecholamine levels in the hemolymph of tobacco hornworm larvae, Manduca sexta, parasitized by the braconid wasp, Cotesia congregata, and in the developing parasitoids. Arch Insect Biochem Physiol 38:193–201
Horton DR, Redak RA (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263–275
Jermy T, Hanson FE, Dethier VG (1968) Induction of specific food preference in lepidopterous larvae. Entomol Exp Appl 11:211–230
Kester KM, Peterson SC, Hanson F, Jackson M, Severson RF (2002) The roles of nicotine and natural enemies in determining larval feeding site distributions of Manduca sexta L., and Manduca quinquemaculata (Haworth) on tobacco. Chemoecology 12:1–10
Kloppenburg P, Hilderbrand JG (1995) Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta. J Exp Biol 198:603–611
Kostal V, Noguchi H, Shimada K, Hayakawa Y (1999) Dopamine and sserotonin in the larval CNS of a drosophilid fly, Chymonyza costata. Are they involved in the regulation of diapause?. Arch Insect Biochem Physiol 42:147–162
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
Leffingwell JC (1999) Leaf chemistry. Basic chemical constituents of tobacco leaf and differences among tobacco types. In: Davis DL, Nielsen MT (eds) Tobacco production, chemistry and technology. Blackwell, London, pp 265–284
Lindroth RL, Osier TL, Barnhill HRH, Wood SA (2002) Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem Syst Ecol 30:297–307
Nakamatsu Y, Tanaka T (2002) Larvae of an endoparasitoid, Cotesia Kariyai (Braconidae: Hymenoptera), feed on the host fat body directly in the second stadium with the help of teratocytes. J Insect Physiol 48:1041–1052
Nakamatsu Y, Tanaka T (2004) Correlation between concentration of hemolymph nutrients and amount of fat body consumed in lightly and heavily parasitized hosts Pseudaletia separata. J Insect Physiol 50:135–141
Noguchi H, Hayakawa Y (1996) Mechanism of parasitism-induced elevation of dopamine levels in host insect larvae. Insect Biochem Molec Biol 26:659–665
Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomol Exp Appl 62:221–231
Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10:151–179
Raubenheimer D, Simpson SJ (1999) Integrating nutrition: a geometric approach. Entomol Exp Appl 91:67–82
Raubenheimer D, Simpson SJ (2003) Nutrient balancing in grasshoppers: behavioural and physiological correlates of dietary breadth. J Exp Biol 206:1669–1681
Rogers SM, Newland PL (2003) The neurobiology of taste in insects. Adv Insect Physiol 31:141–204
Schoonhoven LM (1969) Gustation and foodplant selection in some lepidopterous larvae. Entomol Exp Appl 12:555–564
Schoonhoven LM (1973) Plant recognition by lepidopterous larvae. In: van Emden HF (ed) Insect/plant relationships. Blackwell Scientific, Oxford, pp 87–99
Schoonhoven LM (1987) What makes a caterpillar eat? The sensory code underlying feeding behavior. In: Chapman RF, Bernays EA, Stoffolano JG (eds) Chemoreception and behavior. Springer, Berlin Heidelberg New York, pp 69–97
Schoonhoven LM, Jermy T, van Loon JJA (1998) Insect-plant biology: from physiology to evolution. Chapman and Hall, New York
Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211
Simmonds MSJ, Simpson SJ, Blaney WM (1992) Dietary selection behaviour in Spodoptera littoralis: the effects of conditioning diet and conditioning period on neural responsiveness and selection behaviour. J Exp Biol 162:73–90
Simpson SJ, Raubenheimer D (1993) The central role of the haemolymph in the regulation of nutrient intake in insects. Physiol Entomol 18:395–403
Simpson SJ, Simpson CL (1992) Mechanisms controlling modulation by haemolymph amino acids of gustatory responsiveness in the locust. J Exp Biol 168:269–287
Simpson SJ, Simmonds MSJ, Blaney WM (1988) A comparison of dietary selection behaviour in larval Locusta migratoria and Spodoptera littoralis. Physiol Entomol 13:225–238
Simpson SJ, James S, Simmonds MSJ, Blaney WM (1991) Variation in chemosensitivity and the control of dietary selection behaviour in the locust. Appetite 17:141–154
Simpson SJ, Raubenheimer D, Chambers PG (1995) The mechanism of nutritional homeostasis. In: Chapman RF, DeBoer G (eds) Regulating mechanisms of insect feeding. Chapman and Hall, New York, pp 251–278
Slansky F, Wheeler GS (1991) Food consumption and utilization responses to dietary dilution with cellulose and water by velvetbean caterpillars, Anticarsia gemmatalis. Physiol Entomol 16:99–116
Stockhoff BA (1993) Ontogenetic change in dietary selection for protein and lipid by gypsy moth larvae. J Insect Physiol 39:677–686
Suomela J, Suominen O, Torvi M (1997) Variation in quality of mountain birch and tea-leaved willow for mammal and insect herbivores: differences among trees, among sites and between species. Ecography 20:224–232
Telang A, Booton V, Chapman RF, Wheeler DE (2001) How female caterpillars accumulate their nutrient reserves. J Insect Physiol 47:1055–1064
Thimann KV (1980) The senescence of leaves. In: Thimann KV (ed) Senescence in plants. CRC Press, Boca Raton, pp 85–115
Thompson SN (2004) Dietary fat mediates hyperglycemia and the glucogenic response to increased protein consumption in an insect, Manduca sexta L. Biochim Biophys Acta 1673:208–216
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
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
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
Timmons WA, Reynolds SE (1992) Physiological mechanisms underlying the control of meal size in Manduca sexta larvae. Physiol Entomol 17:81–89
Timmons 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
Trumper S, Simpson SJ (1993) Regulation of salt intake by nymphs of Locusta migratoria. J Insect Physiol 39:857–864
Tso TC (1972) Physiology and biochemistry of tobacco plants. Dowden, Hutchinson and Ross, Stroudsburg, pp 140–145
Waldbauer GP, Friedman S (1991) Self-selection of optimal diets by insects. Annu Rev Entomol 36:43–63
Waldbauer GP, Cohen RW, Friedman S (1984) Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earworm, Heliothis zea (Boddie). Physiol Zool 57:590–597
Yamamoto RT (1969) Mass rearing of the tobacco hornworm. II. Larval rearing and pupation. J Econ Entomol 62:1427–1431
Yamamoto RT, Fraenkel GS (1960) The specificity of the tobacco hornworm, Protoparce sexta, to solanaceous plants. Annu Entomol Soc Am 53:503–507
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Thompson, S.N., Redak, R.A. Feeding behaviour and nutrient selection in an insect Manduca sexta L. and alterations induced by parasitism. J Comp Physiol A 191, 909–923 (2005). https://doi.org/10.1007/s00359-005-0013-5
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DOI: https://doi.org/10.1007/s00359-005-0013-5