Capacity for sustained terrestrial locomotion in an insect: Energetics, thermal dependence, and kinematics

Summary

The capacity for sustained, terrestrial locomotion in the cockroach. Blaberus discoidalis, was determined in relation to running speed, metabolic cost, aerobic capacity, and ambient temperature (T a=15, 23, and 34°C; acclimation temperature=24°C). Steady-state thoracic temperature (T tss) increased linearly with speed at each T a.The difference between T tss and T awas similar at each experimental temperature with a maximum increase of 7°C. Steady-state oxygen consumption (VO2ss) increased linearly with speed at each T aand had a low thermal dependence (Q10=1.0-1.4). The minimum cost of locomotion (the slope of the VO2ss versus speed function) was independent of T a.Cockroaches attained a maximal oxygen consumption (VO2max). increased with T afrom 2.1 ml O2·g-1·h-1 at 15°C to 4.9 ml O2·g-1·h-1 at 23°C, but showed no further increase at 34°C, VO2max increased 23-fold over resting VO2 at 23°C, 10-fold at 34°C, and 15-fold at 15°C. Endurance correlated with the speed at which VO2max was attained (MAS, maximal aerobic speed). Temperature affected the kinematics of locomotion. compared to cockroaches running at the same speed, but higher temperatures (23–34°C), low temperature (15°C) increased protraction time, reduced stride frequency, and reduced stability by increasing body pitching. The thermal independence of the minimum cost of locomotion (Cmin), the low thermal dependence of VO2ss (i.e., y-intercept of the VO2ss versus speed function), and a typical Q10 of 2.0 for VO2max combined to increase MAS and endurance in B. discoidalis when T awas increased from 15 to 23°C. Exerciserelated endothermy enabled running cockroaches to attain a greater VO2max, metabolic scope, and endurance capacity at 23°C than would be possible if T tss remained equal to T a. The MAS of B. discoidalis was similar to that of other arthropods that use trachea, but was 2-fold greater than ectotherms, such as salamanders, frogs, and crabs of a comparable body mass.

This is a preview of subscription content, access via your institution.

Abbreviations

T a :

ambient temperature

T t :

thoracic temperature

T tss :

steady state thoracic temperature during exercise

T trest :

thoracic temperature during rest

VO2 :

oxygen consumption

VO2rest :

oxygen consumption during rest

VO2ss :

steady-state oxygen consumption during exercise

VO2max :

maximal oxygen consumption; MAS maximum aerobic speed

C min :

minimum cost of locomotion

t end :

endurance time

References

  1. Bartholomew GA (1981) Matter of size: an examination of endothermy in insects and terrestrial vertebrates. In: Insect thermoregulation. John Wiley & Sons, New York, pp 45–78

    Google Scholar 

  2. Bartholomew GA, Casey TM (1977a) Endothermy during terrestrial activity in large beetles. Science 195:882–883

    Google Scholar 

  3. Bartholomew GA, Casey TM (1977b) Body temperature and oxygen consumption during rest and activity in relationship to body size in some tropical beetles. J Therm Biol 2:173–176

    Google Scholar 

  4. Bartholomew GA, Heinrich B (1978) Endothermy in African dung betles during flight, ball making, and ball rolling. J Exp Biol 73:65–83

    Google Scholar 

  5. Bartholomew GA, Lighton JRB (1985) Ventilation and oxygen consumption during rest and locomotion in a tropical cockroach, Blaberus giganteus. J Exp Biol 118:449–454

    Google Scholar 

  6. Bartholomew GA, Lighton JRB (1986) Endothermy and energy metabolism of a giant tropical fly, Pantopthalmus tabaninus Thunberg. J Comp Physiol B 156:461–467

    Google Scholar 

  7. Bartholomew GA, Vleck O, Vleck CM (1981) Instantaneous measurements of oxygen consumption during pre-flight warm up and post-flight cooling in sphingid and saturniid moths. J Exp Biol 90:17–32

    Google Scholar 

  8. Baust JC, Miller LK (1970) Variations in glycerol content and its influence on cold hardiness in the Alaskan carabid beetle, Pterostichus brevicornis. J Insect Physiol 16:979–990

    Google Scholar 

  9. Bennett AF (1982) The energetics of reptilian activity. In: Gans C, Pough FH (eds) Biology of Reptilia, vol 13. Academic Press, New York, pp 155–199

    Google Scholar 

  10. Bennett AF, John-Alder HB (1984) The effect of body temperature on the locomotory energetics of lizards. J Comp Physiol B 155:21–27

    Google Scholar 

  11. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654

    Google Scholar 

  12. Casey TM, Hegel-Little JR (1987) Instantaneous oxygen consumption and muscle stroke work in Malacosoma americanum during pre-flight warm-up. J Exp Biol 127:389–400

    Google Scholar 

  13. Casey TM, Joos BA (1983) Morphometrics, conductance, thoracic temperature, and flight energetics of noctuid and geometrid moths. Physiol Zool 56:160–173

    Google Scholar 

  14. Chappell MA (1982) Temperature regulation of carpenter bees (Xylocopa californica) foraging in the Colorado desert of southern California. Physiol Zool 55:267–280

    Google Scholar 

  15. Chappell MA (1984) Thermoregulation and energetics of the green fig beetle (Cotinus texana) during flight and foraging behavior. Physiol Zool 57:581–589

    Google Scholar 

  16. Edney EB (1971) The body temperature of tenebrionid beetles in the Namib Desert of southern Africa. J Exp Biol 55:253–272

    Google Scholar 

  17. Full RJ (1986) Locomotion without lungs: energetics and performance of a lungless salamander, Plethodon jordani. Am J Physiol 251:R775-R780

    Google Scholar 

  18. Full RJ (1987) Locomotion energetics of the ghost crab I. Metabolic cost and endurance. J Exp Biol 130:137–153

    Google Scholar 

  19. Full RJ (1989) Mechanics and energetics of terrestrial locomotion: bipeds to polypeds. In: Wieser W, Gnaiger E (eds) Energy transformation in cells and animals. Thieme, Stuttgart, pp 175–182

    Google Scholar 

  20. Full RJ (1990) Concepts of efficiency and economy in land locomotion. In: Blake R (ed) Efficiency, economy and related concepts in comparative animal physiology. Cambridge University Press, New York, in press

    Google Scholar 

  21. Full RJ, Anderson BD, Finnerty CM, Feder ME (1988) Exercising with and without lungs. I. The effects of metabolic cost, maximal oxygen transport and body size on terrestrial locomotion in salamander species. J Exp Biol 38:471–485

    Google Scholar 

  22. Full RJ, Zuccarello DA, Tullis A (1990) Effect of variation in form on the cost of terrestrial locomotion. J Exp Biol 150:233–296

    Google Scholar 

  23. Guthrie DM, Tindall AR (1968) Biology of the cockroach. St. Martin's Press, New York, pp 10–11

    Google Scholar 

  24. Heinrich B (1970) Thoracic temperature stabilization by blood circulation in a free-fling moth. Science 168:580–582

    Google Scholar 

  25. Heinrich B (1972) Physiology of brood incubation in the bumblebee queen, Bombus vosnesenskii. Nature 239:223–224

    Google Scholar 

  26. Heinrich B (1974) Thermoregulation in endothermic insects. Science 185:747–756

    Google Scholar 

  27. Heinrich B, Buchmann SL (1986) Thermoregulatory physiology of the carpenter bee, Xylocopa varipuncta. J Comp Physiol B 156:557–562

    Google Scholar 

  28. Heinrich B, McClain E (1986) “Laziness” and hypothermia as a foraging strategy in flower scarabs (Coleoptera: Scarabaeidae). Physiol Zool 59:273–282

    Google Scholar 

  29. Herried CF, Full RJ (1984) Cockroaches on a treadmill aerobic running. J Insect Physiol 30:395–403

    Google Scholar 

  30. Herried CF, Prawel DA, Full RJ (1981a) Energetics of running cockroaches. Science 212:331–333

    Google Scholar 

  31. Herried CF, Full RJ, Prawel DA (1981b) Energetics of cockroach locomotion. J Exp Biol 94:189–202

    Google Scholar 

  32. Jensen TF, Holm-Jensen I (1980) Energetic cost of running in workers of three ant species Formica fusca L., Formica rufa L., and Camponotus herculaneaus L. (Hymenoptera, Formicidae). J Comp Physiol 137:151–156

    Google Scholar 

  33. John-Alder HB, Bennett AF (1981) Thermal dependence of endurance and locomotory energetics in a lizard. Am J Physiol 241:R342-R349

    Google Scholar 

  34. John-Alder HB, Lowe CH, Bennett AF (1983) Thermal dependence of locomotory energetics and aerobic capacity of the Gila Monster (Heloderma suspectum). J Comp Physiol 151:119–126

    Google Scholar 

  35. Josephson RK (1981) Temperature-and the mechanical performance of insect muscle. In: Insect thermoregulation. (ed.) (B Heinrich) John Wiley & Sons, New York, pp 19–44

    Google Scholar 

  36. Kammer AE (1981) Physiological mechanisms of thermoregulation. In: Heinrich B (ed) Insect thermoregulation. John Wiley & Sons, New York, pp 115–158

    Google Scholar 

  37. Lighton JRB (1985) Cost of transport and ventilatory patterns in three African beetles. Physiol Zool 58:390–399

    Google Scholar 

  38. Lighton JRB, Bartholomew GA, Feener DH (1987) Energetics of locomotion and load carriage in the leaf-cutting ant Atta colombica. Guer. Physiol Zool 60:524–537

    Google Scholar 

  39. McConnell E, Richards AG (1955) How fast can a cockroach run? Bull Brooklyn Ento Soc 50:36–43

    Google Scholar 

  40. Moberly WR (1968) The metabolic responses of the common iguana, Iguana iguana, to walking and running. Comp Biochem Physiol 27:21–32

    Google Scholar 

  41. Morgan KR (1987) Temperature regulation, energy metabolism and mate searching in rain beetles (Plecoma sp.), winter-active, endothermic scarabs (Coleoptera). J Exp Biol 128:107–122

    Google Scholar 

  42. Morgan KR, Bartholomew GA (1982) Heterothermic response to reduced ambient temperature in a scarab beetle. Science 216:1409–1410

    Google Scholar 

  43. Morgan KR, Heinrich B (1987) Temperature regulation in bee-and wasp-mimicking syrphid flies. J Exp Biol 133:59–71

    Google Scholar 

  44. Morrissey R, Edwards JS (1979) Neural function in an alpine grylloblattid: a comparison with the house cricket, Acheta domesticus. Physiol Entomol 4:241–250

    Google Scholar 

  45. Nicolson SW, Louw GN (1982) Simultaneous measurement of evaporative water loss, oxygen consumption, and thoracic temperature during flight in a carpenter bee. J Exp Zool 222:287–296

    Google Scholar 

  46. Rome LC (1982) Energetic cost of running with different muscle temperatures in Savannah Monitor lizards. J Exp Biol 99:269–277

    Google Scholar 

  47. Seeherman HJ, Taylor CR, Maloiy CMO, Armstrong RB (1981) Design of the mammalian respiratory system: measuring maximum aerobic capacity. Respir Physiol 44:11–24

    Google Scholar 

  48. Seeherman HJ, Dmi'el R, Gleeson TT (1983) Oxygen consumption and lactate production in varanid and iguanid lizards: a mammalian relationship. Int Ser Sport Sci 13:421–427

    Google Scholar 

  49. Shapley H (1924) Note on the thermokinetics of Dolichordrine ants. Prot Natl Acad Sci USA 10:436–439

    Google Scholar 

  50. Taylor CR, Schmidt-Nielson K, Raab JL (1970) Scaling of energetic cost of running to body size in mammals. Am J Physiol 219:1104–1107

    Google Scholar 

  51. Taylor CR, Heglund NC, Maloiy GMO (1982) Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J Exp Biol 97:1–21

    Google Scholar 

  52. Willmer PG (1982) Thermoregulatory mechanisms in Sarcophaga. Oceologia 53:382–385

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Robert J. Full.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Full, R.J., Tullis, A. Capacity for sustained terrestrial locomotion in an insect: Energetics, thermal dependence, and kinematics. J Comp Physiol B 160, 573–581 (1990). https://doi.org/10.1007/BF00258985

Download citation

Key words

  • Endurance
  • Locomotion
  • Energetics Temperature
  • Insects