Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T23:53:18.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Chemical interaction between the larva of a dipteran parasitoid and its coleopteran host: A case of exploitation of the communication system during the searching behaviour?

Published online by Cambridge University Press:  30 November 2011

H.F. Groba  and
M.K. Castelo
H.F. Groba*
Affiliation:
CONICET, Grupo de Investigación en Ecofisiología de Parasitoides (GIEP), Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, Pabellón II, (C1428EHA) Ciudad de Buenos Aires, Argentina
M.K. Castelo
Affiliation:
CONICET, Grupo de Investigación en Ecofisiología de Parasitoides (GIEP), Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Universitaria, Pabellón II, (C1428EHA) Ciudad de Buenos Aires, Argentina
*
*Author for correspondence Fax: (+54-11) 4576-3384 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The robber fly Mallophora ruficauda is one of the principal apicultural pests in the Pampas region of Argentina. As adults, the flies prey on honey bees and other insects; while, as larvae, they parasitize scarab beetle larvae. Females of M. ruficauda lay eggs away from the host in tall grasses. After being dispersed by the wind, larvae drop to the ground, where they dig in search of their hosts. It is known that second instar larvae of M. ruficauda exhibit active host searching behaviour towards its preferred host, third instar larva of Cyclocephala signaticollis, using host-related chemical cues. Furthermore, previous works show that these chemical cues are produced in the posterior body half of hosts. However, the precise anatomical origin of these cues and whether they mediate any behaviour of C. signaticollis larvae remains yet unknown. In order to determine the precise origin of the chemical cue, we carried out olfactometer assays with different stimuli of extracts of the posterior C. signaticollis body half. Additionally, we tested whether C. signaticollis is attracted to any of the same extracts as in the previous experiments. We found that both second instar of M. ruficauda and third instar of C. signaticollis are attracted to extracts of the fermentation chamber (proctodeum). This is the first report of attraction of conspecific larvae in scarab beetles. We discuss a possible case of system communication exploitation in an immature parasitoid-host system.

Keywords

host locationparasitoidAsilidaeScarabaeidaeinfochemicals
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 3 , June 2012 , pp. 315 - 323
Copyright
Copyright © Cambridge University Press 2011

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

Aldrich, J.R. (1995) Chemical communication in the true bugs and parasitoid exploitation. pp. 318–363in Cardé, R.G. & Bell, W.J. (Eds) Chemical Ecology of Insect 2. New York, USA, Chapman & Hall.CrossRefGoogle Scholar
Alvarado, L. (1980) Sistemática y bionomía de los estados inmaduros de coleópteros Scarabaeidae que habitan en el suelo. PhD thesis, Universidad Nacional de la Plata, La Plata, Argentina.Google Scholar
Amat, I., Castelo, M.K., Desouhant, E. & Bernstein, C. (2006) The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia 148, 153–161.CrossRefGoogle ScholarPubMed
Bauchop, T. & Clarke, R.T.J. (1975) Gut microbiology and carbohydrate digestion in the larva of Costelytra zealandica (Coleoptera: Scarabaeidae). New Zealand Journal Zoology 2, 237–243.CrossRefGoogle Scholar
Bidla, G., Hauling, T., Dushay, M.S. & Theopold, U. (2009) Activation of insect phenoloxidase after injury: endogenous versus foreign elicitors. Journal of Innate Immunity 1, 301–308.CrossRefGoogle ScholarPubMed
Bottrell, D.G. & Barbosa, P. (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annual Review of Entomology 43, 347–367.CrossRefGoogle ScholarPubMed
Brodeur, J. & Boivin, G. (2004) Functional ecology of immature parasitoids. Annual Review of Entomology 49, 27–49.CrossRefGoogle ScholarPubMed
Byers, J.A. & Wood, D.L. (1981) Antibiotic-induced inhibition of pheromone synthesis in a bark beetle. Science 213(14), 763–764.CrossRefGoogle Scholar
Capinera, J.L. (1980) A trail pheromone from silk produced by larvae of the range caterpillar Hemileuca oliviae (Lepidoptera: Staruniidae) and observations on aggregation behavior. Journal of Chemical Ecology 6(3), 655–664.CrossRefGoogle Scholar
Castelo, M.K. (2003) Comportamiento de localización y patrones de explotación de hospedadores (Coleoptera: Scarabaeidae) por el moscardón cazador de abejas Mallophora ruficauda (Diptera: Asilidae). PhD thesis, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales. Ciudad Autónoma de Buenos Aires, Argentina.Google Scholar
Castelo, M.K. & Capurro, A.F. (2000) Especificidad y denso-dependencia inversa en parasitoides con oviposición fuera del hospedador: el caso de Mallophora ruficauda (Diptera: Asilidae) en la pampa argentina. Ecología Austral 10, 89–101.Google Scholar
Castelo, M.K. & Corley, J.C. (2004) Oviposition behavior in the robber fly Mallophora ruficauda (Diptera: Asilidae). Annals of the Entomological Society of America 97(4), 1050–1054.CrossRefGoogle Scholar
Castelo, M.K. & Lazzari, C.R. (2004) Host-seeking behavior in larvae of the robber fly Mallophora ruficauda (Diptera: Asilidae). Journal of Insect Physiology 50, 331–336.CrossRefGoogle ScholarPubMed
Castelo, M.K., Ney-Nifle, M., Corley, J.C. & Bernstein, C. (2006) Oviposition height increases parasitism success by the robber fly Mallophora ruficauda (Diptera: Asilidae). Behavioral Ecology and Sociobiology 61, 231–243.CrossRefGoogle Scholar
Cazemier, A.E., Hackstein, J.H.P., Op den Camp, H.L.M., Rosenberg, J. & van der Drift, C. (1997) Bacteria in the intestinal tract of different species of arthropods. Microbiology Ecology 33, 189–197.CrossRefGoogle ScholarPubMed
Chapman, R.F. (1998) The Insect: Structure and Function. 4th edn.Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Copello, A. (1922) Biología del moscardón cazador de abejas (Mallophora ruficauda Wiederman). Physis 6, 30–42.Google Scholar
Coulibaly, A.K. & Fanti, P. (1992) Influence de l'age des oeufs microtypiques suivant les premiers jours de la ponte sur les pourcentages de parasitisme dans le systeme Galleria mellonella L. Pseudogonia fufifrons Wied. Bollettino dell'Istituto di Entomologia “Guido Grandi” della Università degli Studi di Bologna 46, 239–249.Google Scholar
Crespo, J.E. (2011) Ecología y fisiología del comportamiento de localización del hospedador en el parasitoide Mallophora ruficauda. PhD thesis, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales. Ciudad Autónoma de Buenos Aires, Argentina.Google Scholar
Crespo, J.E. & Castelo, M.K. (2008) The ontogeny of host-seeking behaviour in a parasitoid dipteran. Journal of Insect Physiology 54, 842–847.CrossRefGoogle Scholar
De Moraes, C.M., Lewis, J.W. & Tumlinson, J.H. (2000) Examining plant-parasitoid interactions in tritrophic systems. Anais da Sociedade Entomológica do Brasil 29(2), 189–203.CrossRefGoogle Scholar
Deneubourg, J.L., Gregoire, J.C. & Le Fort, E. (1990) Kinetics of larval gregarious behavior in the bark beetle Dendroctonus micans (Coleoptera: Scolytidae). Journal of Insect Behavior 3(2), 169–182.CrossRefGoogle Scholar
Despland, E. & Le Huu, A. (2006) Pros and cons of group living in the forest tent caterpillar: separating the roles of silk and of grouping. Entomologia Experimentalis et Applicata 122, 181–189.CrossRefGoogle Scholar
Dicke, M. (1988) Microbial allelochemicals affecting the behavior of insects, mites, nematodes, and protozoa in different trophic levels. pp. 125–163in Barbosa, P. & Letourneau, D.K. (Eds) Novel Aspects of Insect-Plant Interactions. New York, USA, Wiley.Google Scholar
Dicke, M. & Grostal, P. (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Annual Review of Ecology and Systematics 32, 1–23.CrossRefGoogle Scholar
Dicke, M. & Sabelis, M.W. (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Functional Ecology 2, 131–139.CrossRefGoogle Scholar
Duthie, B., Gries, G., Gries, R., Krupke, C. & Derksen, S. (2003) Does pheromone-based aggregation of codling moth larvae help procure future mates? Journal of Chemical Ecology 29(2), 425–436.CrossRefGoogle ScholarPubMed
Egert, M., Stingl, U., Bruun, L.D., Pommerenke, B., Brune, A. & Friedrich, M.W. (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Applied and Environmental Microbiology 71(8), 4556–4566.CrossRefGoogle Scholar
Eggleton, P. & Belshaw, R. (1992) Insect Parasitoids: An Evolutionary Overview. Philosophical Transactions of the Royal Society of London 337, 1–20.Google Scholar
Eggleton, P. & Belshaw, R. (1993) Comparisons of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biological Journal of the Linnean Society 48, 213–226.CrossRefGoogle Scholar
Feener, D.H. Jr & Brown, B.V. (1997) Diptera as parasitoids. Annual Review of Entomology 42, 73–97.CrossRefGoogle ScholarPubMed
Fehlbaum, P., Bulet, P., Michaut, L., Largueux, M., Broekaert, W.F., Hetru, C. & Hoffmann, J.A. (1994) Septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. The Journal of Biological Chemistry 269(52), 33159–33163.CrossRefGoogle ScholarPubMed
Greenfield, M.D. (2002) Signallers and Receivers: Mechanisms and Evolution of Arthropod Communication. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Ghent, A.W. (1960) A study of the group-feeding behaviour of larvae of the jack pine sawfly, Neodiprion pratti banksianae Roh. Behaviour 16(1/2), 110–148.CrossRefGoogle Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavior and Evolutionary Ecology. Princeton, NJ, USA, Princeton University Press.CrossRefGoogle Scholar
Hoyt, C.P., Osborne, G.O. & Mulcock, A.P. (1971) Production of an insect sex attractant by symbiotic bacteria. Nature 230(16), 472–473.CrossRefGoogle ScholarPubMed
Hunter, A.F. (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91(2), 213–224.CrossRefGoogle Scholar
Inouye, B.D. & Johnson, D.M. (2005) Larval aggregation affects feeding rate in Chlosyne poecile (Lepidoptera: Nymphalidae). The Florida Entomologist 88(3), 247–252.CrossRefGoogle Scholar
Jumean, Z., Fazel, L., Wood, C., Cowan, T., Eveden, M.L. & Gries, G. (2009) Cocoon-spinning larvae of oriental fruit moth and indianmeal moth do not produce aggragation pheromone. Agricultural and Forest Entomology 11, 205–212.CrossRefGoogle Scholar
Leal, W.S. (1998) Chemical ecology of phytophagous scarab beetles. Annual Reviews of Entomology 43, 39–61.CrossRefGoogle ScholarPubMed
Lewis, W.J. & Martin, W.R. (1990) Semiochemicals for use with parasitoids: status and future. Journal of Chemical Ecology 16, 3067–3089.CrossRefGoogle Scholar
López, A.N., Alvarez Castillo, H.A., Carmona, D., Manetti, P.L. & Vincini, A.M. (1994) Aspectos morfológicos y biológicos de Cyclocephala signaticollis Burm. (Coleoptera: Scarabaeidae). Centro Regional Buenos Aires Sur (CERBAS) INTA-Estación Experimental Agropecuaria, Balcarce. Boletín Técnico 123, 18 pp.Google Scholar
López-Guerrero, Y. & Morón, M.A. (1990) Estudio morfológico e histológico del aparato digestivo larvario de Dynastes hyllus Chevr. (Coleoptera: Melolonthidae, Dynastinae). Folia Entomológica Mexicana 79, 65–83.Google Scholar
Ma, P.W.K. & Ramaswamy, S.B. (2003) Biology and ultrastructure of sex pheromone-producing tissue. pp. 19–51in Blomquist, G. & Vogt, R. (Eds) Insect Pheromone Biochemistry and Molecular Biology: The Biosynthesis and Detection of Pheromones and Plant Volatiles. London, UK, Elsevier.CrossRefGoogle Scholar
Potter, D.A. (1981) Seasonal emergence and flight of northern and southern masked chafers in relation to air and soil temperature and rainfall patterns. Environmental Entomology 10, 793–797.CrossRefGoogle Scholar
Rabinovich, M. & Corley, J.C. (1997) An important new predator of honeybees. the robber fly Mallophora ruficauda Wiedemann (Diptera-Asilidae) in Argentina. American Bee Journal 137(4), 303–306.Google Scholar
Riba, J.M. & Blas, M. (1995) Entomofauna asociada a Trypodendron lineatum (Olivier, 1975) (Coleoptera, scolytidae). Orsis 10, 105–122.Google Scholar
Roitberg, B.D., Sircom, J., Roitberg, C.A., van Alphen, J.J.M. & Mangel, M. (1993) Life expectancy and reproduction. Nature 364, 108.CrossRefGoogle ScholarPubMed
Rosner, B. (1995) Fundamentals of Biostatistics. 4th edn.Belmont, CA, USA, Duxbury Press.Google Scholar
Ruzicka, Z. & Zemek, R. (2008) Deterrent effects of larval tracks on conspecific larvae in Cycloneda limbifer. BioControl 53, 763–771.CrossRefGoogle Scholar
Stamp, N.E. & Bowers, M.D. (1990) Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71(3), 1031–1039.CrossRefGoogle Scholar
Sokal, R.R. & Rohlf, F.J. (1969) Biometry. 1st edn.New York, USA, W.H. Freeman.Google Scholar
Steidle, J.L.M. & van Loon, J.J.A. (2003) Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomologia Experimentalis et Applicata 108, 133–148.CrossRefGoogle Scholar
Stireman III, J.O., O'Hara, J.E. & Monty Wood, D. (2006) Tachinidae: evolution, behavior, and ecology. Annual Review of Entomology 51, 525–555.CrossRefGoogle Scholar
Stowe, M.K., Turlings, T.C.J., Loughrin, J.H., Lewis, W.J. & Tumlinson, J.H. (1995) The chemistry of eavesdropping, alarm and deceit. Proceedings of the National Academy of Sciences of the United State of America 92, 23–28.CrossRefGoogle ScholarPubMed
Tillman, J.A., Seybold, S.J., Jurenka, R.A. & Blomquist, G.J. (1999) Insect pheromones – an overview of biosynthesis and endocrine regulation. Insect Biochemistry and Molecular Biology 29, 481–514.CrossRefGoogle ScholarPubMed
Tsubaki, Y. & Shiotsu, Y. (1982) Group feeding as a strategy for exploiting food resources in the burnet moth Pryeria sinica. Oecologia 55, 12–20.CrossRefGoogle ScholarPubMed
Vet, L.E.M. (1999) From chemical to population infochemical use in an evolutionary context. Journal of Chemical Ecology 25(1), 31–49.CrossRefGoogle Scholar
Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141–172.CrossRefGoogle Scholar
Vet, L.E.M., Wäckers, F.L. & Dicke, M. (1991) How to hunt for hiding host: the reliability-detectability problem in foraging parasitoids. Netherlands Journal of Zoology 41, 202–213.CrossRefGoogle Scholar
Vet, L.E.M., Lewis, W.J. & Cardé, R.T. (1995) Parasitoid foraging and learning. pp. 65–101in Cardé, R.T. & Bell, W.J. (Eds) Chemical Ecology of Insects 2. New York, USA, Chapman & Hall.CrossRefGoogle Scholar
Villani, M.G. & Wright, R.J. (1990) Environmental influences on soil macroarthropod behavior in agricultural system. Annual Review of Entomology 35, 249–269.CrossRefGoogle Scholar
Wajnberg, E., Bernhard, P., Hamelin, F. & Boivin, G. (2006) Optimal patch time allocation for time-limited foragers. Behavioral Ecology and Sociobiology 60, 1–10.CrossRefGoogle Scholar
Wertheim, B. (2005) Evolutionary ecology of communication signals that induce aggregative behaivour. Oikos 109, 117–124.CrossRefGoogle Scholar
Wertheim, B., van Baalen, E.A., Dicke, M. & Vet, L.E.M. (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annual Review of Entomology 50, 321–346.CrossRefGoogle ScholarPubMed
Wiskerke, J.S.C., Dicke, M. & Vet, L.E.M. (1993) Drosophila parasitoid solves foraging problem through infochemical detour: the role adult fly pheromone. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society Amsterdam 4, 79–84.Google Scholar
Wright, E.J. & Müller, P. (1989) Laboratory studies of host finding, acceptance and suitability of the dung-breeding fly Haematobia thirouxi potans (Dipt.: Muscidae) by Aleochara sp. (Col.: Staphylinidae). Entomophaga 34(2), 61–71.CrossRefGoogle Scholar
Wyatt, T.D. (2003) Pheromones and Animal Behavior: Communication by Smell and Taste. Edinburgh, UK, Cambridge University Press.CrossRefGoogle Scholar
Zar, J.H. (1984) Biostatistical Analisys. Englewood Cliffs, NJ, USA, Prentice-Hall International.Google Scholar