Scaling of resting and maximum hopping metabolic rate throughout the life cycle of the locust Locusta migratoria

Journal of Experimental Biology

Volumn 214, Issue 19, 2011, Pages 3218-3224

  Snelling, Edward P ^a   Seymour, Roger S ^a   Matthews, Philip G D ^b   Runciman, Sue ^c   White, Craig R ^b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c FLINDERS UNIVERSITY   (Australia)

Author keywords

Allometry; Fractal network model; Hopping; Insect; Locust; Maximum metabolic rate; Respirometry; Weight

Indexed keywords

ANIMAL; ARTICLE; AUSTRALIA; BODY WEIGHT; ENERGY METABOLISM; FEMALE; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; LOCOMOTION; LOCUST; MALE; OXYGEN CONSUMPTION; PHYSIOLOGY; SEX DIFFERENCE;

ANIMALS; AUSTRALIA; BODY WEIGHT; ENERGY METABOLISM; FEMALE; LIFE CYCLE STAGES; LOCOMOTION; LOCUSTA MIGRATORIA; MALE; OXYGEN CONSUMPTION; SEX FACTORS;

HEXAPODA; LOCUSTA MIGRATORIA; ORTHOPTERA;

EID: 80052642168     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.058420     Document Type: Article

References (60)

1. Addo-Bediako, A., Chown, S. L. and Gaston, K. J. (2002). Metabolic cold adaptation in insects: a large-scale perspective. Funct. Ecol. 16, 332-338. (Pubitemid 34667665)
2. Bailey, C. G. and Riegert, P. W. (1973). Energy dynamics of Encoptolophus sordidus costalis (Scudder) (Orthoptera: Acrididae) in a grassland ecosystem. Can. J. Zool. 51, 91-100.
3. Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2002). Supply-demand balance and metabolic scaling. Proc. Natl. Acad. Sci. USA 99, 10506-10509.
4. Banavar, J. R., Moses, M. E., Brown, J. H., Damuth, J., Rinaldo, A., Sibly, R. M. and Maritan, A. (2010). A general basis for quarter-power scaling in animals. Proc. Natl. Acad. Sci. USA 107, 15816-15820.
5. Barbosa, L. A., Garcia, G. J. M. and da Silva, J. K. L. (2006). The scaling of maximum and basal metabolic rates of mammals and birds. Physica A 359, 547-554. (Pubitemid 41526268)
6. Bartholomew, G. A. and Casey, T. M. (1978). Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J. Exp. Biol. 76, 11-25.
7. Bartholomew, G. A., Lighton, J. R. B. and Feener, D. H. (1988). Energetics of trail running, load carriage, and emigration in the column-raiding army ant Eciton hamatum. Physiol. Zool. 61, 57-68.
8. Beenakkers, A. M. T., Vanderhorst, D. J. and Vanmarrewijk, W. J. A. (1984). Insect flight muscle metabolism. Insect Biochem. 14, 243-260.
9. Bishop, C. M. (1999). The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc. R. Soc. Lond. B 266, 2275-2281.
10. Brown, J. H., West, G. B. and Enquist, B. J. (2005). Yes, West, Brown and Enquist's model of allometric scaling is both mathematically correct and biologically relevant. Funct. Ecol. 19, 735-738. (Pubitemid 41805971)
11. Chappell, M. A., Bailey, N. W., Redak, R. A., Antolin, M. and Zuk, M. (2009). Metabolic similarity despite striking behavioral divergence: aerobic performance in lowand high-density forms of the Mormon cricket. Physiol. Biochem. Zool. 82, 405-418.
12. Chown, S. L., Gibbs, A. G., Hetz, S. K., Klok, C. J., Lighton, J. R. B. and Marais, E. (2006). Discontinuous gas exchange in insects: a clarification of hypotheses and approaches. Physiol. Biochem. Zool. 79, 333-343.
13. Chown, S. L., Marais, E., Terblanche, J. S., Klok, C. J., Lighton, J. R. B. and Blackburn, T. M. (2007). Scaling of insect metabolic rate is inconsistent with the nutrient supply network model. Funct. Ecol. 21, 282-290. (Pubitemid 46426603)
14. Contreras, H. L. and Bradley, T. J. (2009). Metabolic rate controls respiratory pattern in insects. J. Exp. Biol. 212, 424-428.
15. Darveau, C. A., Suarez, R. K., Andrews, R. D. and Hochachka, P. W. (2002). Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166-170. (Pubitemid 34506795)
16. Gouveia, S. M., Simpson, S. J., Raubenheimer, D. and Zanotto, F. P. (2000). Patterns of respiration in Locusta migratoria nymphs when feeding. Physiol. Entomol. 25, 88-93. (Pubitemid 30165794)
17. Greenlee, K. J. and Harrison, J. F. (2004a). Development of respiratory function in the American locust Schistocerca americana I. Across-instar effects. J. Exp. Biol. 207, 497-508. (Pubitemid 38162385)
18. Greenlee, K. J. and Harrison, J. F. (2004b). Development of respiratory function in the American locust Schistocerca americana II. Within-instar effects. J. Exp. Biol. 207, 509-517. (Pubitemid 38162386)
19. Greenlee, K. J., Henry, J. R., Kirkton, S. D., Westneat, M. W., Fezzaa, K., Lee, W. K. and Harrison, J. F. (2009). Synchrotron imaging of the grasshopper tracheal system: morphological and physiological components of tracheal hypermetry. Am. J. Physiol. 297, 1343-1350.
20. Harrison, J. F., Phillips, J. E. and Gleeson, T. T. (1991). Activity physiology of the twostriped grasshopper, Melanoplus bivittatus: gas exchange, hemolymph acid-base status, lactate production, and the effect of temperature. Physiol. Zool. 64, 451-472.
21. Harrison, J. F., Lafreniere, J. J. and Greenlee, K. J. (2005). Ontogeny of tracheal dimensions and gas exchange capacities in the grasshopper, Schistocerca americana. Comp. Biochem. Physiol. 141A, 372-380. (Pubitemid 41225432)
22. Hetz, S. K. and Bradley, T. J. (2005). Insects breathe discontinuously to avoid oxygen toxicity. Nature 433, 516-519. (Pubitemid 40204307)
23. Katz, S. L. and Gosline, J. M. (1993). Ontogenic scaling of jump performance in the African desert locust (Schistocerca gregaria). J. Exp. Biol. 177, 81-111.
24. Kirkton, S. D. and Harrison, J. F. (2006). Ontogeny of locomotory behaviour in the American locust, Schistocerca americana: from marathoner to broad jumper. Anim. Behav. 71, 925-931.
25. Kirkton, S. D., Niska, J. A. and Harrison, J. F. (2005). Ontogenetic effects on aerobic and anaerobic metabolism during jumping in the American locust, Schistocerca americana. J. Exp. Biol. 208, 3003-3012. (Pubitemid 41265190)
26. Komai, Y. (1998). Augmented respiration in a flying insect. J. Exp. Biol. 201, 2359-2366. (Pubitemid 28422374)
27. Kozlowski, J. and Konarzewski, M. (2004). Is West, Brown and Enquist's model of allometric scaling mathematically correct and biologically relevant? Funct. Ecol. 18, 283-289. (Pubitemid 38504291)
28. Kram, R. (1996). Inexpensive load carrying by rhinoceros beetles. J. Exp. Biol. 199, 609-612. (Pubitemid 126603891)
29. Lighton, J. R. B. (1996). Discontinuous gas exchange in insects. Annu. Rev. Entomol. 41, 309-324. (Pubitemid 126640171)
30. Lighton, J. R. B., Bartholomew, G. A. and Feener, D. H. (1987). Energetics of locomotion and load carriage and a model of the energy cost of foraging in the leafcutting ant Atta columbica Guer. Physiol. Zool. 60, 524-537.
31. Lighton, J. R. B., Weier, J. A. and Feener, D. H. (1993). The energetics of locomotion and load carriage in the desert harvester ant Pogonomyrmex rugosus. J. Exp. Biol. 181, 49-61.
32. Mizisin, A. P. and Ready, N. E. (1986). Growth and development of flight muscle in the locust (Schistocerca nitens, Thunberg). J. Exp. Zool. 237, 45-55. (Pubitemid 16154988)
33. Nespolo, R. F., Castaneda, L. E. and Roff, D. A. (2005). The effect of fasting on activity and resting metabolism in the sand cricket, Gryllus firmus: a multivariate approach. J. Insect Physiol. 51, 61-66. (Pubitemid 40427914)
34. Newsholme, E. A., Beis, I., Leech, A. R. and Zammit, V. A. (1978). Role of creatine kinase and arginine kinase in muscle. Biochem. J. 172, 533-537. (Pubitemid 8375834)
35. Niven, J. E. and Scharlemann, J. P. W. (2005). Do insect metabolic rates at rest and during flight scale with body mass? Biol. Lett. 1, 346-349. (Pubitemid 41374900)
36. Price, C. A., Enquist, B. J. and Savage, V. M. (2007). A general model for allometric covariation in botanical form and function. Proc. Natl. Acad. Sci. USA 104, 13204-13209. (Pubitemid 351737617)
37. Queathem, E. (1991). The ontogeny of grasshopper jumping performance. J. Insect Physiol. 37, 129-138.
38. Quinlan, M. C. and Gibbs, A. G. (2006). Discontinuous gas exchange in insects. Respir. Physiol. Neurobiol. 154, 18-29. (Pubitemid 44666579)
39. Riveros, A. J. and Enquist, B. J. (2011). Metabolic scaling in insects supports the predictions of the WBE model. J. Insect Physiol. 57, 688-693.
40. Savage, V. M., Gillooly, J. F., Woodruff, W. H., West, G. B., Allen, A. P., Enquist, B. J. and Brown, J. H. (2004). The predominance of quarter-power scaling in biology. Funct. Ecol. 18, 257-282. (Pubitemid 38504290)
41. Schneider, A., Wiesner, R. J. and Grieshaber, M. K. (1989). On the role of arginine kinase in insect flight muscle. Insect Biochem. 19, 471-480.
42. Seymour, R. S., Withers, P. C. and Weathers, W. W. (1998). Energetics of burrowing, running, and free-living in the Namib Desert golden mole (Eremitalpa namibensis). J. Zool. 244, 107-117. (Pubitemid 28165078)
43. Snelling, E. P., Seymour, R. S., Runciman, S., Matthews, P. G. D. and White, C. R. (2011). Symmorphosis and the insect respiratory system: allometric variation. J. Exp. Biol. 214, 3225-3237.
44. Socha, J. J., Forster, T. D. and Greenlee, K. J. (2010). Issues of convection in insect respiration: insights from synchrotron X-ray imaging and beyond. Respir. Physiol. Neurobiol. 173, S65-S73.
45. Strauss, K. and Reinhold, K. (2010). Scaling of metabolic rate in the lesser wax moth Achroia grisella does not fit the 3/4-power law and shows significant sex differences. Physiol. Entomol. 35, 59-63.
46. Suarez, R. K. and Darveau, C. A. (2005). Multi-level regulation and metabolic scaling. J. Exp. Biol. 208, 1627-1634. (Pubitemid 40697611)
47. Terblanche, J. S., Klok, C. J. and Chown, S. L. (2004). Metabolic rate variation in Glossina pallidipes (Diptera: Glossinidae): gender, ageing and repeatability. J. Insect Physiol. 50, 419-428. (Pubitemid 38583501)
48. Weibel, E. R. and Hoppeler, H. (2005). Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J. Exp. Biol. 208, 1635-1644. (Pubitemid 40697612)
49. Weibel, E. R., Taylor, C. R. and Hoppeler, H. (1991). The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc. Natl. Acad. Sci. USA 88, 10357-10361. (Pubitemid 21915834)
50. Weibel, E. R., Taylor, C. R. and Bolis, L. (1998). Principles of Animal Design: The Optimization and Symmorphosis Debate. Cambridge: Cambridge University Press.
51. Weibel, E. R., Bacigalupe, L. D., Schmitt, B. and Hoppeler, H. (2004). Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir. Physiol. Neurobiol. 140, 115-132. (Pubitemid 38595259)
52. West, G. B., Brown, J. H. and Enquist, B. J. (1997). A general model for the origin of allometric scaling laws in biology. Science 276, 122-126. (Pubitemid 27161259)
53. West, G. B., Brown, J. H. and Enquist, B. J. (1999). The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677-1679. (Pubitemid 29291379)
54. West, G. B., Savage, V. M., Gillooly, J., Enquist, B. J., Woodruff, W. H. and Brown, J. H. (2003). Why does metabolic rate scale with body size? Nature 421, 713-713.
55. Westneat, M. W., Betz, O., Blob, R. W., Fezzaa, K., Cooper, W. J. and Lee, W. K. (2003). Tracheal respiration in insects visualized with synchrotron X-ray imaging. Science 299, 558-560. (Pubitemid 36135151)
56. White, C. R. and Seymour, R. S. (2005). Allometric scaling of mammalian metabolism. J. Exp. Biol. 208, 1611-1619. (Pubitemid 40697609)
57. White, C. R., Phillips, N. F. and Seymour, R. S. (2006). The scaling and temperature dependence of vertebrate metabolism. Biol. Lett. 2, 125-127. (Pubitemid 43384691)
58. Withers, P. C. (2001). Design, calibration and calculation for flow-through respirometry systems. Aust. J. Zool. 49, 445-461. (Pubitemid 33001817)
59. Worm, R. A. A. and Beenakkers, A. M. T. (1980). Regulation of substrate utilization in the flight muscle of the locust, Locusta migratoria, during flight. Insect Biochem. 10, 53-59.
60. Zar, J. H. (1998). Biostatistical Analysis. Englewood Cliffs, NJ: Prentice Hall.