Intraspecific scaling and early life history determine the cost of free-flight in a large beetle (Batocera rufomaculata)

Tomer Urca , Eran Levin , Eran Gefen , Gal Ribak

Insect Science ›› 2024, Vol. 31 ›› Issue (2) : 524 -532.

PDF
Insect Science ›› 2024, Vol. 31 ›› Issue (2) : 524 -532. DOI: 10.1111/1744-7917.13250
ORIGINAL ARTICLE

Intraspecific scaling and early life history determine the cost of free-flight in a large beetle (Batocera rufomaculata)

Author information +
History +
PDF

Abstract

The scaling of the energetic cost of locomotion with body mass is well documented at the interspecific level. However, methodological restrictions limit our understanding of the scaling of flight metabolic rate (MR) in free-flying insects. This is particularly true at the intraspecific level, where variation in body mass and flight energetics may have direct consequences for the fitness of an individual. We applied a 13C stable isotope method to investigate the scaling of MR with body mass during free-flight in the beetle Batocera rufomaculata. This species exhibits large intraspecific variation in adult body mass as a consequence of the environmental conditions during larval growth. We show that the flight-MR scales with body mass to the power of 0.57, with smaller conspecifics possessing up to 2.3 fold higher mass-specific flight MR than larger ones. Whereas the scaling exponent of free-flight MR was found to be like that determined for tethered-flight, the energy expenditure during free-flight was more than 2.7 fold higher than for tethered-flight. The metabolic cost of flight should therefore be studied under free-flight conditions, a requirement now enabled by the 13C technique described herein for insect flight.

Keywords

allometry / body mass / Coleoptera / free-flight / insect flight / stable carbon isotope / tethered-flight

Cite this article

Download citation ▾
Tomer Urca, Eran Levin, Eran Gefen, Gal Ribak. Intraspecific scaling and early life history determine the cost of free-flight in a large beetle (Batocera rufomaculata). Insect Science, 2024, 31(2): 524-532 DOI:10.1111/1744-7917.13250

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahmed,K.U., Rahman, M.M., Alam,M.Z., Hossain,M.M. and Miah, M.G. (2014) Evaluation of relative host preference of Batocera rufomaculata De geer on different age stages of jackfruit trees. Asian Journal of Scientific Research, 7, 232–237.

[2]

Bartholomew,G.A. and Barnhart, M.C. (1984) Tracheal gases, respiratory gas exchange, body temperature and flight in some tropical cicadas. Journal of Experimental Biology, 111, 131–144.

[3]

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. Journal of Experimental Biology, 76, 11–25.

[4]

Ben-Yehuda,S., Dorchin, Y. and Mendel,Z. (2000) Outbreaks of the fig borer Batocera rufomaculata and other cerambycids in fruit plantations in Israel. Alon Hanotea, 54, 23–29.

[5]

Boggs,C.L. and Freeman, K.D. (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia, 144, 353–361.

[6]

Boggs,C.L. and Niitepõld, K. (2016) Effects of larval dietary restriction on adult morphology, with implications for flight and life history. Entomologia Experimentalis Et Applicata, 159, 189–196.

[7]

Bonner,N. and Peters, R.H. (2006) The ecological implications of body size. Journal of Applied Ecology, 22, 291.

[8]

Brown,S., Soroker, V. and Ribak,G. (2017) Effect of larval growth conditions on adult body mass and long-distance flight endurance in a wood-boring beetle: do smaller beetles fly better? Journal of Insect Physiology, 98, 327–335.

[9]

Callier,V. and Nijhout, H.F. (2011) Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proceedings of the National Academy of Sciences USA, 108, 14664–14669.

[10]

Casey,T.M., May,M.L. and Morgan,K.R. (1985) Flight energetics of euglossine bees in relation to morphology and wing stroke frequency. Journal of Experimental Biology, 116, 271–289.

[11]

Chappell,M.A. and Morgan, K.R. (1987) Temperature regulation, endothermy, resting metabolism, and flight energetics of tachinid flies (Nowickia sp.). Physiological Zoology, 60, 550–559.

[12]

Darveau,C.A., Billardon, F. and Belanger,K. (2014) Intraspecific variation in flight metabolic rate in the bumblebee Bombus impatiens: repeatability and functional determinants in workers and drones. Journal of Experimental Biology, 217, 536–544.

[13]

Davidowitz,G., D'amico, L.J. and Nijhout,H.F. (2004) The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research, 6, 49–62.

[14]

Dudley,R. (2000) The Biomechanics of Insect Flight: Form, Function, Evolution. Princeton University Press.

[15]

Dudley,R. and Ellington, C.P. (1990) Mechanics of forward flight in bumblebees: I. Kinematics and morphology. Journal of Experimental Biology, 148, 19–52.

[16]

Ellington,C., Machin, K. and Casey,T. (1990) Oxygen consumption of bumblebees in forward flight. Nature, 347, 472–473.

[17]

Ellington,C.P. (1984a) The aerodynamics of hovering insect flight. VI. Lift and power requirements. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 305, 145–181.

[18]

Ellington,C.P. (1984b) The aerodynamics of hovering insect flight. III. Kinematics. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 305, 41–78.

[19]

Ellington,C.P. (1985) Power and efficiency of insect flight muscle. Journal of Experimental Biology, 115, 293–304.

[20]

Foucart,T., Lourdais, O., DeNardo,D.F. and Heulin,B. (2014) Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara. Journal of Experimental Biology, 217, 4049–4056.

[21]

Glazier,D.S. (2005) Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biological Reviews, 80, 611.

[22]

Grula,C.C., Rinehart, J.P., Greenlee,K.J. and Bowsher,J.H. (2021) Body size allometry impacts flight-related morphology and metabolic rates in the solitary bee Megachile rotundata. Journal of Insect Physiology, 133, 104275.

[23]

Harrison,J.F., Kaiser, A. and VandenBrooks,J.M. (2010) Atmospheric oxygen level and the evolution of insect body size. Proceedings of the Royal Society B: Biological Sciences, 277, 1937–1946.

[24]

Hayward,A. and Gillooly, J.F. (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE, 6, e16557.

[25]

Hechinger,R.F., Sheehan, K.L. and Turner,A.V (2019) Metabolic theory of ecology successfully predicts distinct scaling of ectoparasite load on hosts. Proceedings of the Royal Society B: Biological Sciences, 286, 20191777.

[26]

Heinrich,B. (1971) Temperature regulation of the Sphinx Moth, Manduca Sexta: I. Flight energetics and body temperature during free and tethered flight. Journal of Experimental Biology, 54, 141–152.

[27]

Hicks,O., Burthe, S.J., Daunt,F., Newell,M., Butler, A., Ito,M. et al. (2018) The energetic cost of parasitism in a wild population. Proceedings of the Royal Society B: Biological Sciences, 285, 20180489.

[28]

Horne,C.R., Hirst,A.G. and Atkinson,D. (2015) Temperature-size responses match latitudinal-size clines in arthropods, revealing critical differences between aquatic and terrestrial species. Ecology Letters, 18, 327–335.

[29]

Husain,M.A. and Khan, M.A.W. (1940) Bionomics and control of the fig-tree borer, Batocera rufomaculata De Geer (Coleoptera: Lamiidae). The Indian Journal of Agricultural Sciences, 10, 945–959.

[30]

Hvas,M. and Oppedal, F. (2019) Influence of experimental set-up and methodology for measurements of metabolic rates and critical swimming speed in Atlantic salmon Salmo salar. Journal of Fish Biology, 95, 893–902.

[31]

Langellotto,G.A., Denno, R.F. and Ott,J.R. (2000) A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. Ecology, 81, 865–875.

[32]

Late,T., Krogh,A. and Weis-Fogh,T. (1951) The respiratory exchange of the desert locust (Schistocerca gregaria) before, during and after flight. Journal of Experimental Biology, 28, 344–357.

[33]

Lehmann,F.O. and Heymann, N. (2006) Dynamics of in vivo power output and efficiency of Nasonia asynchronous flight muscle. Journal of Biotechnology, 124, 93–107.

[34]

Lehmann,F.O., Dickinson, M.H. and Staunton,J. (2000) The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.). Journal of Experimental Biology, 203, 1613–1624.

[35]

McCullough,E.L., Weingarden, P.R. and Emlen,D.J. (2012) Costs of elaborate weapons in a rhinoceros beetle: how difficult is it to fly with a big horn? Behavioral Ecology, 23, 1042–1048.

[36]

Niven,J.E. and Scharlemann, J.P.W. (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biology Letters, 1, 346–349.

[37]

Pennycuick,C.J. (1969) The mechanics of bird migration. Ibis, 111, 525–556.

[38]

Pyke,G.H., Pulliam, H.R. and Charnov,E.L. (1977) Optimal foraging: a selective review of theory and tests. The Quarterly Review of Biology, 52, 137–154.

[39]

Ribak,G., Barkan, S. and Soroker,V. (2017) The aerodynamics of flight in an insect flight-mill. PLoS ONE, 12, e0186441.

[40]

Roberts,S.P., Harrison, J.F. and Dudley,R. (2004) Allometry of kinematics and energetics in carpenter bees (Xylocopa varipuncta) hovering in variable-density gases. Journal of Experimental Biology, 207, 993–1004.

[41]

Schmidt-Nielsen,K. (1972) Locomotion: energy cost of swimming, flying, and running. Science, 177, 222–228.

[42]

Snelling,E.P., Seymour, R.S., Matthews,P.G.D. and White,C.R. (2012) Maximum metabolic rate, relative lift, wingbeat frequency, and stroke amplitude during tethered-flight in the adult locust Locusta migratoria. Journal of Experimental Biology, 215, 3317–3323.

[43]

Tanaka,S. and Suzuki, Y. (1998) Physiological trade-offs between reproduction, flight capability and longevity in a wing-dimorphic cricket, Modicogryllus confirmatus. Journal of Insect Physiology, 44, 121–129.

[44]

Urca,T. and Ribak, G. (2021) The relationship between body size and flight power output in the Mango stem borer (Batocera rufomaculata). Journal of Insect Physiology, 133, 104290.

[45]

Urca,T., Levin,E. and Ribak,G. (2021) Insect flight metabolic rate revealed by bolus injection of the stable isotope 13C. Proceedings of the Royal Society B: Biological Sciences, 288, 20211082.

[46]

Urca,T., Levin,E. and Ribak,G. (2022) Metabolic cost of flight and aerobic efficiency in the rose chafer, Protaetia cuprea (Cetoniinae). Insect Science, 29, 1361–1372.

RIGHTS & PERMISSIONS

2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

212

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/