Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-12-01T03:09:08.776Z Has data issue: false hasContentIssue false
  • English
  • Français

Energy allocation during the maturation of adults in a long-lived insect: implications for dispersal and reproduction

Published online by Cambridge University Press:  09 July 2015

G. David ,
B. Giffard ,
I. van Halder ,
D. Piou  and
H. Jactel
G. David*
Affiliation:
INRA, UMR1202 BIOGECO, F-33610, Cestas, France University of Bordeaux, BIOGECO, UMR1202, F-33600, Pessac, France
B. Giffard
Affiliation:
INRA, UMR1202 BIOGECO, F-33610, Cestas, France University of Bordeaux, BIOGECO, UMR1202, F-33600, Pessac, France Bordeaux Sciences Agro, University of Bordeaux, 1 Cours du Général de Gaulle, F-33170 Gradignan, France
I. van Halder
Affiliation:
INRA, UMR1202 BIOGECO, F-33610, Cestas, France University of Bordeaux, BIOGECO, UMR1202, F-33600, Pessac, France
D. Piou
Affiliation:
INRA, UMR1202 BIOGECO, F-33610, Cestas, France University of Bordeaux, BIOGECO, UMR1202, F-33600, Pessac, France Département de la Santé des Forêts, Ministère de l'Agriculture, de l'Alimentation et de la Pêche, DGAL-SDQPV, Paris F-75732, France
H. Jactel
Affiliation:
INRA, UMR1202 BIOGECO, F-33610, Cestas, France University of Bordeaux, BIOGECO, UMR1202, F-33600, Pessac, France
*
*Authors for correspondence Phone: +33 5 57 12 27 37 Fax: +33 5 57 12 27 81 Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Energy allocation strategies have been widely documented in insects and were formalized in the context of the reproduction process by the terms ‘capital breeder’ and ‘income breeder’. We propose here the extension of this framework to dispersal ability, with the concepts of ‘capital disperser’ and ‘income disperser’, and explore the trade-off in resource allocation between dispersal and reproduction. We hypothesized that flight capacity was sex-dependent, due to a trade-off in energy allocation between dispersal and egg production in females. We used Monochamus galloprovincialis as model organism, a long-lived beetle which is the European vector of the pine wood nematode. We estimated the flight capacity with a flight mill and used the number of mature eggs as a proxy for the investment in reproduction. We used the ratio between dry weights of the thorax and the abdomen to investigate the trade-off. The probability of flying increased with the adult weight at emergence, but was not dependent on insect age or sex. Flight distance increased with age in individuals but did not differ between sexes. It was also positively associated with energy allocation to thorax reserves, which increased with age. In females, the abdomen weight and the number of eggs also increase with age with no negative effect on flight capacity, indicating a lack of trade-off. This long-lived beetle has a complex strategy of energy allocation, being a ‘capital disperser’ in terms of flight ability, an ‘income disperser’ in terms of flight performance and an ‘income breeder’ in terms of egg production.

Keywords

allocation strategiesflight capacityMonochamus galloprovincialisdispersal–reproduction trade-off
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 629 - 636
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akbulut, S., Keten, A. & Stamps, W.T. (2008) Population dynamics of Monochamus galloprovincialis Olivier (Coleoptera: Cerambycidae) in two pine species under laboratory conditions. Journal of Pest Science 81, 115–121.CrossRefGoogle Scholar
Amat, I., Besnard, S., Foray, V., Pelosse, P., Bernstein, C. & Desouhant, E. (2012) Fuelling flight in a parasitic wasp: which energetic substrate to use? Ecological Entomology 37, 480–489.Google Scholar
Atkins, M.D. (1961) A study of the flight of the douglas-fir beetle Dendroctonus pseudotsugae hopk. (Coleoptera: Scolytidae): iii flight capacity. The Canadian Entomologist 93, 467–474.CrossRefGoogle Scholar
Beenakkers, A.M.T., Van der Horst, D.J. & Van Marrewijk, W.J.A. (1984) Insect flight muscle metabolism. Insect Biochemistry 14, 243–260.Google Scholar
Begon, M., Townsend, C.R. & Harper, J.L. (2009) Ecology: From Individuals to Ecosystems. Malden, MA, John Wiley & Sons.Google Scholar
Boggs, C.L. (1981) Nutritional and life-history determinants of resource allocation in holometabolous insects. The American Naturalist 117, 692–709.Google Scholar
Boggs, C. & Ross, C. (1993) The effect of adult food limitation on life-history traits in Speyeria mormonia (Lepidoptera, Nymphalidae). Ecology 74, 433–441.Google Scholar
Candy, D.J., Becker, A. & Wegener, G. (1997) Coordination and integration of metabolism in insect flight. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 117, 497–512.Google Scholar
Casas, J., Pincebourde, S., Mandon, N., Vannier, F., Poujol, R. & Giron, D. (2005) Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 86, 545–554.Google Scholar
Chapman, R.F., Simpson, S.J. & Douglas, A.E. (2013) The Insects: Structure and Function. New York, Cambridge University Press.Google Scholar
Cheng, H.R., Lin, M., Li, W. & Fang, Z. (1983) The occurrence of a pine wilting disease caused by a nematode found in Nanjing. Forest Pest and Disease 4, 1–5.Google Scholar
Coll, M. & Yuval, B. (2004) Larval food plants affect flight and reproduction in an oligophagous insect herbivore. Environmental Entomology 33, 1471–1476.Google Scholar
Crawley, M.J. (2012) The R Book. Chichester, West Sussex, England, John Wiley & Sons.Google Scholar
David, G., Giffard, B., Piou, D. & Jactel, H. (2014) Dispersal capacity of Monochamus galloprovincialis, the European vector of the pine wood nematode, on flight mills. Journal of Applied Entomology 138, 566–576.CrossRefGoogle Scholar
Dixon, A.F.G., Horth, S. & Kindlmann, P. (1993) Migration in insects: cost and strategies. Journal of Animal Ecology 62, 182–190.CrossRefGoogle Scholar
Edwards, J.S. (1961) On the reproduction of Prionoplus reticularis (Coleoptera, Cerambycidae), with general remarks on reproduction in the Cerambycidae. Quarterly Journal of Microscopical Science s3–102, 519–529.Google Scholar
Ellers, J. & Van Alphen, J.J.M. (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. Journal of Evolutionary Biology 10, 771–785.Google Scholar
Evans, H.F., McNamara, D.G., Braasch, H., Chadoeuf, J. & Magnusson, C. (1996) Pest Risk Analysis (PRA) for the territories of the European Union (as PRA area) on Bursaphelenchus xylophilus and its vectors in the genus Monochamus. EPPO Bulletin 26, 199–249.Google Scholar
Fadamiro, H.Y., Chen, L., Onagbola, E.O. & Graham, L. (2005) Lifespan and patterns of accumulation and mobilization of nutrients in the sugar-fed phorid fly, Pseudacteon tricuspis . Physiological Entomology 30, 212–224.Google Scholar
Fischer, H. & Kutsch, W. (2000) Relationships between body mass, motor output and flight variables during free flight of juvenile and mature adult locusts, Schistocerca gregaria . Journal of Experimental Biology 203, 2723–2735.Google Scholar
Gäde, G. & Auerswald, L. (2000) Flight substrates and their regulation by a member of the AKH/RPCH family of neuropeptides in Cerambycidae. Journal of Insect Physiology 46, 1575–1584.Google Scholar
Gäde, G. & Auerswald, L. (2002) Beetles’ choice—proline for energy output: control by AKHs. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 132, 117–129.Google Scholar
Glazier, D.S. (1999) Trade-offs between reproductive and somatic (storage) investments in animals: a comparative test of the Van Noordwijk and De Jong model. Evolutionary Ecology 13, 539–555.Google Scholar
Guerra, P.A. (2011) Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biological Reviews 86, 813–835.Google Scholar
Gu, H., Hughes, J. & Dorn, S. (2006) Trade-off between mobility and fitness in Cydia pomonella L. (Lepidoptera: Tortricidae). Ecological Entomology 31, 68–74.Google Scholar
Hanski, I., Saastamoinen, M. & Ovaskainen, O. (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. Journal of Animal Ecology 75, 91–100.CrossRefGoogle Scholar
Hughes, J. & Dorn, S. (2002) Sexual differences in the flight performance of the oriental fruit moth, Cydia molesta . Entomologia experimentalis et applicata 103, 171–182.Google Scholar
Ims, R.A. (1995) Movement patterns related to spatial structures. pp. 85–109 in Hansson, L., Fahrig, L. & Merriam, G. (ed) Mosaic Landscapes and Ecological Processes. The Netherlands, Springer.Google Scholar
Jactel, H. & Gaillard, J. (1991) A preliminary study of the dispersal potential of Ips sexdentatus (Boern) (Col., Scolytidae) with an automatically recording flight mill. Journal of Applied Entomology 112, 138–145.CrossRefGoogle Scholar
Jervis, M.A., Boggs, C.L. & Ferns, P.N. (2005) Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecological Entomology 30, 359–375.Google Scholar
Jervis, M.A., Boggs, C.L. & Ferns, P.N. (2007) Egg maturation strategy and survival trade-offs in holometabolous insects: a comparative approach. Biological Journal of the Linnean Society 90, 293–302.Google Scholar
Jervis, M.A., Ellers, J. & Harvey, J.A. (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53, 361–385.Google Scholar
Johnson, C.G. (1969) Migration and dispersal of insects by flight. London, John Wiley & Son.Google Scholar
Khuhro, N.H., Biondi, A., Desneux, N., Zhang, L., Zhang, Y. & Chen, H. (2014) Trade-off between flight activity and life-history components in Chrysoperla sinica . BioControl 59, 219–227.Google Scholar
Lieutier, F., Day, K.R., Battisti, A., Gregoire, J.-C. & Evans, H.F. (2004) Bark and Wood Boring Insects in Living Trees in Europe: A Synthesis. Dordrecht, Netherlands, Springer.Google Scholar
Marden, J.H. (2000) Variability in the size, composition, and function of insect flight muscles. Annual Review of Physiology 62, 157–178.Google Scholar
Mole, S. & Zera, A.J. (1994) Differential resource consumption obviates a potential flight–fecundity trade-off in the sand cricket (Gryllus firmus). Functional Ecology 8, 573–580.Google Scholar
Naves, P., Sousa, E. & Quartau, J. (2006a) Reproductive traits of Monochamus galloprovincialis (Coleoptera: Cerambycidae) under laboratory conditions. Bulletin of Entomological Research 96, 289–294.Google Scholar
Naves, P., Sousa, E. & Quartau, J. (2006b) Feeding and oviposition preferences of Monochamus galloprovincialis for certain conifers under laboratory conditions. Entomologia Experimentalis et Applicata 120, 99–104.Google Scholar
Naves, P., Camacho, S., Sousa, E. & Quartau, J. (2007) Transmission of the pine wood nematode Bursaphelenchus xylophilus through feeding activity of Monochamus galloprovincialis (Col., Cerambycidae). Journal of Applied Entomology 131, 21–25.CrossRefGoogle Scholar
Pelosse, P., Jervis, M.A., Bernstein, C. & Desouhant, E. (2011) Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness? Biological Journal of the Linnean Society 104, 621–632.Google Scholar
Rankin, M.A. & Burchsted, J.C.A. (1992) The cost of migration in insects. Annual Review of Entomology 37, 533–559.Google Scholar
Raubenheimer, D. (1995) Problems with ratio analysis in nutritional studies. Functional Ecology 9, 21.Google Scholar
R development core team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria.Google Scholar
Ronce, O. (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annual Review of Ecology, Evolution, and Systematics 38, 231–253.Google Scholar
Sousa, E., Bonifácio, L., Pires, J., Penas, A.C., Mota, M., Bravo, M.A. (2001) Bursaphelenchus xylophilus (Nematoda; Aphelenchoididae) associated with Monochamus galloprovincialis (Coleoptera; Cerambycidae) in Portugal. Nematology 3, 89–91.Google Scholar
Stearns, S.C. (1992) The Evolution of Life Histories. Oxford, University Press Oxford.Google Scholar
Suarez, R.K., Darveau, C.-A., Welch, K.C., O'Brien, D.M., Roubik, D.W. & Hochachka, P.W. (2005) Energy metabolism in orchid bee flight muscles: carbohydrate fuels all. Journal of Experimental Biology 208, 3573–3579.CrossRefGoogle Scholar
Weeda, E., de Kort, C.A.D. & Beenakkers, A.M.T. (1979) Fuels for energy metabolism in the Colorado potato beetle, Leptinotarsa decemlineata Say. Journal of Insect Physiology 25, 951–955.Google Scholar
Zera, A.J. & Denno, R.F. (1997) Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology 42, 207–230.CrossRefGoogle ScholarPubMed
Supplementary material: File

David supplementary material

Appendix 1-2

Download David supplementary material(File)
File 84.5 KB