Metabolic allometry during development and metamorphosis of the silkworm bombyx mori: Analyses, patterns, and mechanisms

Physiological and Biochemical Zoology

Volumn 83, Issue 2, 2010, Pages 215-231

  Blossman Myer, Bonnie L ^a   Burggren, Warren W ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CYTOCHROME C OXIDASE; LIPID;

ALLOMETRY; BODY MASS; DEVELOPMENTAL BIOLOGY; ENZYME ACTIVITY; FUNCTIONAL MORPHOLOGY; GAS EXCHANGE; GROWTH RATE; HISTOLOGY; INTRASPECIFIC INTERACTION; LARVAL DEVELOPMENT; LIPID; METABOLISM; METAMORPHOSIS; MITOCHONDRIAL DNA; MOTH;

ANIMAL; ARTICLE; BODY SURFACE; BODY WATER; CHEMISTRY; DIGESTIVE SYSTEM; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; INSECT; LARVA; METABOLISM; METAMORPHOSIS; MITOCHONDRION; OXYGEN CONSUMPTION; PHYSIOLOGY; SILKWORM;

ANIMALS; BODY SURFACE AREA; BODY WATER; BOMBYX; CARBON DIOXIDE; DIGESTIVE SYSTEM; ELECTRON TRANSPORT COMPLEX IV; LARVA; LIPIDS; METAMORPHOSIS, BIOLOGICAL; MITOCHONDRIA; OXYGEN CONSUMPTION; PUPA;

BOMBYX MORI;

EID: 77749254590     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/648393     Document Type: Article

References (79)

1. Agutter P.S. and D.N. Wheatley. 2004. Metabolic scaling: consensus or controversy? Theor Biol Med Model 16:1-13.
2. Baldwin K.M. and R.S. Hakim. 1991. Growth and differentiation of the larval midgut epithelium during molting in the moth, Manduca sexta. Tissue Cell 23:411-422.
3. Beckage N.E., D.B. Gelman, M.A. Chappell, and M. Alleyne. 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. (Pubitemid 27344964)
4. Bennett V.A., O. Kukal, and R.E. Lee Jr. 1999. Metabolic opportunists: feeding and temperature influence the rate and pattern of respiration in the high arctic woollybear caterpillar Gynaephora groenlandica (Lymantriidae). J Exp Biol 202:47-53.
5. Blossman-Myer B. and W.W. Burggren. 2010. The silk cocoon of the silkworm, Bombyx mori: macro structure and its influence on transmural diffusion of oxygen and water vapor. Comp Biochem Physiol A 155:259-263.
6. Bradley T.J. 1984. Mitochondrial placement and function in insect ion-transporting cells. Am Zool 24:157-167.
7. Burggren W.W. 2005. Developing animals flout prominent assumptions of ecological physiology. Comp Biochem Physiol A 141:430-439.
8. Caǧlayan S.H. 1990. Changes in the chemical composition of fat body during the last larval instar of Manduca sexta. Acta Biol Hung 41:363-372.
9. Canavoso L.E., H.K. Yun, Z.E. Jouni, and M.A. Wells. 2004. Lipid transfer particle mediates the delivery of diacylglycerol from lipophorin to fat body in larval Manduca sexta. J Lipid Res 45:456-465.
10. Chamberlin M.E. 2007. Changes in mitochondrial electron transport chain activity during insect metamorphosis. Am J Physiol 292:R1016-R1022.
11. Chamberlin M.E., C.M. Gibellato, R.J. Noecker, and E.J. Dankoski. 1997. Changes in midgut active ion transport and metabolism during larval-larval molting in the tobacco hornworm (Manduca sexta). J Exp Biol 200:643-648.
12. Chown S.L., A.G. Gibbs, S.K. Hetz, C.J. Klok, J.R.B. Lighton, and E. Marais. 2006. Discontinuous gas exchange in insects: a clarification of hypotheses and approaches. Physiol Biochem Zool 79:333-343.
13. Cloudsley-Thompson J.L. 1975. Adaptations of Arthropoda to arid environments. Annu Rev Entomol 20:261-283.
14. Connor W.E., Y. Wang, M. Green, and D.S. Lin. 2006. Effects of diet and metamorphosis upon the sterol composition of the butterfly Morpho peleides. J Lipid Res 47:1444-1448.
15. Czarnołȩski M., J. Kozłowski, G. Dumiot, J.-C. Bonnet, J. Mallard, and M. Dupont-Nivet. 2008. Scaling of metabolism in Helix aspersa snails: changes through ontogeny and response to selection for increased size. J Exp Biol 211:391-399.
16. Davies R. and C. Moyes. 2007. Allometric scaling in centrarchid fish: origins of intra- and inter-specific variation in oxidative and glycolytic enzyme levels in muscle. J Exp Biol 210:3798-3804.
17. D'Costa M.A. and L.M. Birt. 1966. Changes in the lipid content during the metamorphosis of the blowfly, Lucilia. J Insect Physiol 12:1377-1394.
18. Domroese K.A. and L.I. Gilbert. 1964. The role of lipid in adult development and flight muscle metabolism in Hyalophora cecropia. J Exp Biol 41:573-590.
19. Economo E.P., A.J. Kerkhoff, and B. Enquist. 2005. Allometric growth, life-history invariants and population energetics. Ecol Lett 8:353-360.
20. Edwards J. 1953. Insect Physiology. Wiley, New York.
21. Fast P. 1964. Insect lipids: a review. Mem Entomol Soc Can 37:3-50.
22. Feldman H.A. and T.A. McMahon. 1983. The 3/4 mass exponent for energy metabolism is not a statistical artifact. Respir Physiol 52:149-163.
23. Fernando-Warnakulasuriya G.J.P., K. Tsuchida, and M.A.Wells. 1988. Effect of dietary lipid content on lipid transport and storage during larval development of Manduca sexta. Insect Biochem 18:211-214.
24. Fugo H., S. Hitoshi, N. Hiromichi, and S. Akinori. 1984. Eclosion hormone activity in developing embryos of the silkworm, Bombyx mori. J Insect Physiol 31:293-298.
25. Ganga G. 2003. Comprehensive Sericulture. Vol.2. Silkworm Rearing and Silk Reeling. Science, Enfield, NH.
26. Gibellato C.M. and M.E. Chamberlin. 1994. Midgut metabolism in different instars of the tobacco hornworm (Manduca sexta). J Exp Zool 270:405-409.
27. Glazier D. 2005. Beyond the "3/4-power law": variation in the intra-and interspecific scaling of metabolic rate in animals. Biol Rev Camb Philos Soc 80:661-662.
28. Grant J.B. 2006. Diversification of gut morphology in caterpillars is associated with defensive behavior. J Exp Biol 209: 3018-3024.
29. Gray E.M. and T. J. Bradley. 2006. Evidence from mosquitoes suggest that cyclic gas exchange and discontinuous gas exchange are two manifestations of a single respiratory pattern. J Exp Biol 209:1603-1611.
30. Greenlee K.J. and J.F. Harrison. 2004a. Development of respiratory function in the American locust Schistocerca americana. I. Across-instar effects. J Exp Biol. 207:497-508.
31. -. 2004b. Development of respiratory function in the American locust Schistocerca americana. II. Within-instar effects. J Exp Biol 207:509-517.
32. -. 2005. Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar, Manduca sexta. J Exp Biol 208:1385-1392
33. Harrison J.F., J.J. Lafreniere, and K.J. Greenlee. 2005. Ontogeny of tracheal dimensions and gas exchange capacities in the grasshopper, Schistocerca americana. Comp Biochem Physiol A 141:372-380.
34. Hetz S.K. 2007. The role of the spiracles in gas exchange during development of Samia cynthia (Lepidoptera, Saturniidae). Comp Biochem Physiol A 148:743-754.
35. Hetz S.K. and T.J. Bradley. 2005. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433:516-519.
36. Heusner A.A. 1982. Energy metabolism and body size. I. Is the 0.75 mass exponent of Kleiber's equation a statistical artifact? Respir Physiol 48:1-12.
37. Heyland A. and L.L. Moroz. 2006. Signaling mechanisms underlying metamorphic transitions in animals. Integr Comp Biol 46:743-759.
38. Hulbert A.J. and P.L. Else. 2005. Membranes and the setting of the energy demand. J Exp Biol 208:1593-1599.
39. Hunt von Herbing I. 2006. The physiological basis for metabolic scaling in animals: a developing perspective. Pp. 83-95 in S. Warburton, W.W. Burggren, B. Pelster, C. Reiber, and J. Spicer, eds. Comparative Developmental Physiology. Oxford University Press, New York.
40. Jouni Z.E. and M.A. Wells. 1996. Purification and partial characterization of a lutein-binding protein from the midgut of the silkworm Bombyx mori. J Biol Chem 271:14722-14726.
41. Kemp W.P., J. Bosch, and B. Dennis. 2004. Oxygen consumption during the life cycles of the prepupa-wintering bee Megachile rotundata and the adult-wintering bee Osmia lignaria (Hymenoptera: Megachilidae). Ann Entomol Soc Am 97:161-170.
42. Kleiber M. 1932. Body size and metabolism. Hilgardia 6:315-349.
43. -. 1975. The Fire of Life: An Introduction to Animal Energetics. Rev. ed. Krieger, Huntington, NY.
44. Kozłowski J. and M. Konarzewski. 2004. Is West, Brown and Enquist's model of allometric scaling mathematically correct and biologically relevant? Funct Ecol 18:283-289.
45. Levy R.I. and H.A. Schneiderman. 1966. Discontinuous respiration in insects. IV. Changes in intratracheal pressure during the respiratory cycle of silkworm pupae. J Insect Physiol 12:465-492.
46. Lighton J.R.B. 1996. Discontinuous gas exchange in insects. Annu Rev Entomol 41:309-324
47. Mandel L.J., T.G. Riddle, and J.M. Storey. 1980. Role of ATP in respiratory control and active transport in tobacco hornworm midgut. Am J Physiol 238:C10-C14.
48. Matsuura S., T. Morimoto, S. Nagata, and Y. Tashiro. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori. II. Cytolytic processes in posterior silk gland cells during metamorphosis from larva to pupa. J Cell Biol 38:589-603.
49. Moran D., B. Gara, and R.M.G. Wells. 2007. Energetics and metabolism of yellowtail kingfish (Seriola lalandi Valenciennes 1833) during embryogenesis. Aquaculture 265:359-369. (Pubitemid 46546422)
50. Moran D. and R.M.G. Wells. 2007. Ontogenetic scaling of fish metabolism in the mouse-to-elephant mass magnitude range. Comp Biochem Physiol A 148:611-620.
51. Morimoto T., S. Matsuura, S. Nagata, and Y. Tashiro. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori. III. Ultrastructural changes of posterior silk gland cells in the fourth larval instar. J Cell Biol 38:604-614.
52. Moses M.E., C. Hou, W.H. Woodruff, G.B. West, J.C. Nekola, W. Zuo, and J.H. Brown. 2008. Revisiting a model of ontogenetic growth: estimating model parameters from theory and data. Am Nat 171:632-645.
53. 10) of oxygen consumption in a cricket. J Exp Biol 206:4309-4315.
54. Odell J.P. 1998. Energetics of metamorphosis in two holometabolous insect species: Manduca sexta (Lepidoptera: Sphin gidae) and Tenebrio molitor (Coleoptera: Tenebrionidae). J Exp Zool 280:344-353.
55. Ojeda-Avila T., H.A. Woods, and R.A. Raguso. 2003. Effects of dietary variation on growth, composition, and maturation of Manduca sexta (Sphingidae: Lepidoptera). J Insect Physiol 49:293-306.
56. Parenti P., B. Giordana, V.F. Sacchi, G.M. Hanozet, and A. Guerritore. 1985. Metabolic activity related to the potassium pump in the midgut of Bombyx mori larvae. J Exp Biol 116: 69-78.
57. Patel R.T., J.L. Soulages, B. Hariharasundaram, and E.L. Arrese. 2005. Activation of the lipid droplet controls the rate of lipolysis of triglycerides in the insect fat body. J Biol Chem 280:22624-22631.
58. Powers D.R. and T.M. Conley. 1994. Field metabolic rate and food consumption in two sympatric hummingbird species in southeastern Arizona. Condor 96:141-150.
59. Prasad S.V., R.O. Ryan, J.H. Law, and M.A.Wells. 1986. Changes in lipoprotein composition during larval-pupal metamorphosis of an insect, Manduca sexta. J Biol Chem 261:558-562.
60. Rockstein M. 1973. The Physiology of Insecta. Academic Press, New York.
61. Sasaki S. and Y. Tashiro. 1976. Studies on the posterior silk gland of the silkworm, Bombyx mori. V. Electron microscope localization of fibroin in the posterior silk gland at the later stage of the fifth instar. J Cell Biol 70:648-659.
62. Satake S., Y. Kawabe, and A. Mizoguchi. 2000. Carbohydrate metabolism during starvation in the silkworm Bombyx mori. Arch Insect Biochem Physiol 44:90-98.
63. Schmidt-Nielsen K. 1984. Scaling: Why Is Animal Size So Important? Cambridge University Press, Cambridge.
64. Schroeder L. and D.G. Dunlap. 1970. Respiration of cecropia moth (Hyalophora cecropia L.) larvae. Comp Biochem Physiol 35:953-957.
65. Seibel B.A. 2007. On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the class Cephalopoda (Mollusca). J Exp Biol 210:1-11.
66. Smith R.L. 1984. Allometric scaling in comparative biology: problems of concept and method. Am J Physiol 246:R152-R160.
67. Stusek P., F. Pohleven, and D. Capl. 2000. Detection of wood boring insects by measurement of oxygen consumption. Int Biodeterior Biodegrad 46:293-298.
68. Syed Z., Y. Ishida, K. Taylor, D.A. Kimbrell, and W.S. Leal. 2006. Pheromone reception in fruit flies expressing a moth's odorant receptor. Proc Natl Acad Sci USA 103:16538-16543.
69. Tashiro Y., T. Morimoto, S. Matsuura, and S. Nagata. 1968. Studies on the posterior silk gland of the silkworm, Bombyx mori. I. Growth of posterior silk gland cells and biosynthesis of fibroin during the fifth larval instar. J Cell Biol 38:574-588.
70. Tenney S.M. 1985. Oxygen supply and limiting oxygen pressures in an insect larva. Respir Physiol 60:121-134.
71. Tojo S., T. Betchaku, V.J. Ziccardi, and G.R. Wyatt. 1978. Fat body protein granules and storage proteins in the silkmoth, Hyalophora cecropia. J Cell Biol 78:823-838.
72. Toledo L.E., S.P. Brito, W.K. Milsom, A.S. Abe, and D.V. Andrade. 2008. Effects of season, temperature, and body mass on the standard metabolic rate of tegu lizards (Tupinambis merianae). Physiol Biochem Zool 81:158-164.
73. Uchimura K., H. Ai, K. Kuwasawa, T. Matsushita, and M. Kurakawa. 2005. Excitatory neural control of posterograde heartbeat by the frontal ganglion in the last instar larva of a lepidopteran, Bombyx mori. J Comp Physiol A 192:175-185.
74. Wang Z.-M., R.N. Pierson Jr., and S.B. Heymsfield. 1992. The five-level model: a new approach to organizing bodycomposition research. Am J Clin Nutr 56:19-28.
75. West G.B. and J.H. Brown. 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.
76. West G.B., W.H. Woodruff, and J.H. Brown. 2002. Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc Natl Acad Sci USA 99:2473-2478.
77. s2/3. Proc Natl Acad Sci 100:4046-4049.
78. Wieser W. 1984. A distinction must be made between the ontogeny and the phylogeny of metabolism in order to understand the mass exponent of energy metabolism. Respir Physiol 55:1-9.
79. Withers P.C. 1992. Comparative Animal Physiology. Saunders, Fort Worth, TX.