Skip to main content Accessibility help
×
Home
Hostname: page-component-55597f9d44-jzjqj Total loading time: 0.403 Render date: 2022-08-08T11:16:01.126Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

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*
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: david.guillaume27@gmail.com

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.

Type
Research Papers
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, 115121.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, 480489.CrossRefGoogle 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, 467474.CrossRefGoogle Scholar
Beenakkers, A.M.T., Van der Horst, D.J. & Van Marrewijk, W.J.A. (1984) Insect flight muscle metabolism. Insect Biochemistry 14, 243260.CrossRefGoogle 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, 692709.CrossRefGoogle Scholar
Boggs, C. & Ross, C. (1993) The effect of adult food limitation on life-history traits in Speyeria mormonia (Lepidoptera, Nymphalidae). Ecology 74, 433441.CrossRefGoogle 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, 497512.CrossRefGoogle 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, 545554.CrossRefGoogle 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, 15.Google Scholar
Coll, M. & Yuval, B. (2004) Larval food plants affect flight and reproduction in an oligophagous insect herbivore. Environmental Entomology 33, 14711476.CrossRefGoogle Scholar
Crawley, M.J. (2012) The R Book. Chichester, West Sussex, England, John Wiley & Sons.CrossRefGoogle 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, 566576.CrossRefGoogle Scholar
Dixon, A.F.G., Horth, S. & Kindlmann, P. (1993) Migration in insects: cost and strategies. Journal of Animal Ecology 62, 182190.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 s3102, 519529.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, 771785.CrossRefGoogle 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, 199249.CrossRefGoogle 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, 212224.CrossRefGoogle 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, 27232735.Google ScholarPubMed
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, 15751584.CrossRefGoogle ScholarPubMed
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, 117129.CrossRefGoogle ScholarPubMed
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, 539555.CrossRefGoogle 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, 813835.CrossRefGoogle ScholarPubMed
Gu, H., Hughes, J. & Dorn, S. (2006) Trade-off between mobility and fitness in Cydia pomonella L. (Lepidoptera: Tortricidae). Ecological Entomology 31, 6874.CrossRefGoogle Scholar
Hanski, I., Saastamoinen, M. & Ovaskainen, O. (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. Journal of Animal Ecology 75, 91100.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, 171182.CrossRefGoogle Scholar
Ims, R.A. (1995) Movement patterns related to spatial structures. pp. 85109 in Hansson, L., Fahrig, L. & Merriam, G. (ed) Mosaic Landscapes and Ecological Processes. The Netherlands, Springer.CrossRefGoogle 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, 138145.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, 359375.CrossRefGoogle 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, 293302.CrossRefGoogle Scholar
Jervis, M.A., Ellers, J. & Harvey, J.A. (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53, 361385.CrossRefGoogle ScholarPubMed
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, 219227.CrossRefGoogle 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.CrossRefGoogle Scholar
Marden, J.H. (2000) Variability in the size, composition, and function of insect flight muscles. Annual Review of Physiology 62, 157178.CrossRefGoogle ScholarPubMed
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, 573580.CrossRefGoogle Scholar
Naves, P., Sousa, E. & Quartau, J. (2006a) Reproductive traits of Monochamus galloprovincialis (Coleoptera: Cerambycidae) under laboratory conditions. Bulletin of Entomological Research 96, 289294.CrossRefGoogle ScholarPubMed
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, 99104.CrossRefGoogle 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, 2125.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, 621632.CrossRefGoogle Scholar
Rankin, M.A. & Burchsted, J.C.A. (1992) The cost of migration in insects. Annual Review of Entomology 37, 533559.CrossRefGoogle Scholar
Raubenheimer, D. (1995) Problems with ratio analysis in nutritional studies. Functional Ecology 9, 21.CrossRefGoogle Scholar
R development core team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria.Google ScholarPubMed
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, 231253.CrossRefGoogle 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, 8991.CrossRefGoogle 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, 35733579.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, 951955.CrossRefGoogle Scholar
Zera, A.J. & Denno, R.F. (1997) Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology 42, 207230.CrossRefGoogle ScholarPubMed
Supplementary material: File

David supplementary material

Appendix 1-2

Download David supplementary material(File)
File 84 KB
14
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

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

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

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

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *