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Host gut microorganisms’ cues mediate orientation behaviour in the larva of the parasitoid Mallophora ruficauda

Published online by Cambridge University Press:  02 November 2015

H.F. Groba  and
M.K. Castelo
H.F. Groba*
Affiliation:
Grupo de Investigación en Ecofisiología de Parasitoides (GIEP), Departamento de Ecología, Genética y Evolución- Instituto IEGEBA (CONICET – UBA), 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:
Grupo de Investigación en Ecofisiología de Parasitoides (GIEP), Departamento de Ecología, Genética y Evolución- Instituto IEGEBA (CONICET – UBA), 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 Phone: (+54-11) 4576-3300 E-mail: hernan_groba@yahoo.com.ar
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Abstract

The robber fly Mallophora ruficauda is one of the most important apicultural pests in the Pampas region of Argentina. This species is a parasitoid of scarab beetle larvae. Females lay eggs away from the host, and the larvae perform active search behaviour toward Cyclocephala signaticollis third instar larvae, parasitoid's preferred host. This behaviour is mediated by host-related chemical cues produced in hosts’ fermentation chamber. Also, C. signaticollis larvae are attracted to fermentation chamber extracts. As scarab larvae have microbe-rich fermentation chamber, it has been suggested that microorganisms could be involved in the production of these semiochemicals. The aims of this work were first to ascertain the presence of microorganisms in the fermentation chamber of C. signaticollis larvae and second to determine the role of microorganisms in the orientation response of parasitoid and host larvae. We found that microorganisms-free C. signaticollis larvae showed deterioration in their development and did not produce the attractive semiochemicals. Therefore, we isolated fermentation chamber microorganisms of host larvae by means of different cultures media, and then, assayed different microorganisms’ stimuli by binary choice tests. We were able to isolate microorganisms and determine that M. ruficauda larvae are attracted to semiochemicals from protein degradation in the fermentation chamber. However, C. signaticollis larvae were not attracted to any semiochemicals associated with microorganisms’ activity in the fermentation chamber. Although we were unable to elucidate the exact role of gut microorganisms in host behaviour, we discuss their relevance in parasitoid host-seeking behaviour and host conspecific interaction in M. ruficauda–C. signaticollis system.

Keywords

Asilidaehost locationmicroorganismsparasitoid; Scarabaeidaesemiochemicals
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 1 , February 2016 , pp. 81 - 90
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Copyright © Cambridge University Press 2015 

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References

Afsheen, S., Wang, X., Li, R., Zhu, C. & Lou, Y. (2008) Differential attraction of parasitoid in relation of specificity of kairomones from herbivores and their by-products. Insect Science 15, 381–397.Google Scholar
Aldrich, J.R. (1995) Chemical communication in the true bugs and parasitoid exploitation. pp. 318–363 in Carde, R.T. & Bell, W.J. (Eds) Chemical Ecology of Insect 2. New York, Springer Publishing.Google Scholar
Alvarado, L.J. (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, pp. 199.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.Google Scholar
Bailón Lira, L., Gonzalez Melendez, R.C. & Cervantes Sandoval, A. (2003) Atlas de pruebas Bioquímicas Para Identificar Bacterias. México D.F., Universidad Nacional Autonoma de Mexico, pp. 174.Google Scholar
Barrantes, M.E. & Castelo, M.K. (2014) Host specificity of the larval parasitoid Mallophora ruficauda (Diptera: Asilidae) and the influence of the age on this process. Bulletin of Entomological Research 104(3), 295–306.Google Scholar
Ben-Yosef, M., Aharon, Y., Jurkevitch, E. & Yuval, B. (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. Proceedings of the Royal Society B 277, 1545–1552.Google Scholar
Bernays, E.A. & Klein, B.A. (2002) Quantifying the symbiont contribution to essential amino acids in aphids: the importance of tryptophan for Uroleucon ambrosiae . Physiological Entomology 27, 275–284.Google Scholar
Billen, J. & Buschinger, A. (2000) Morphology and ultrastructure of a specialized bacterial pouch in the digestive tract of Tetraponera ants (Formicidae, Pseudomyrmecinae). Arthropod Structure & Development 29, 259–266.Google Scholar
Boone, C.K., Six, D.L., Zheng, Y. & Raffa, K.F. (2008) Parasitoids and dipteran predators exploit volatiles from microbial symbionts to locate bark beetles. Environmental Entomology 37(1), 150–161.Google Scholar
Brock, T.D., Smith, D.W. & Madigan, M.T. (1987) Microbiologia. Mexico, DF, Prentice-Hall Hispanoamericana, pp. 906.Google Scholar
Brodeur, J. & Boivin, G. (2004) Functional ecology of immature parasitoids. Annual Review of Entomology 49, 27–49.Google Scholar
Bution, M.L. & Caetano, F.H. (2008) Ileum of the Cephalotes ants: a specialized structure to harbor symbionts microorganisms. Micron 39, 897–909.Google 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.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.Google Scholar
Castelo, M.K. & Corley, J.C. (2010) Spatial density-dependent parasitism and specificity in the robber fly Mallophora ruficauda (Diptera: Asilidae). Austral Ecology 35, 72–81.Google 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.Google Scholar
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.Google Scholar
Chandler, S.M., Wilkinson, T.L. & Douglas, A.E. (2008) Impact of plant nutrients on the relationship between an herbivorous insect and its symbiotic bacteria. Proceedings of the Royal Society B 275, 565–570.Google Scholar
Chapman, R.F. (2013) The Insects: Structure and function. Cambridge, Cambridge University Press, pp. 954.Google Scholar
Chaves, S., Neto, M. & Tenreiro, R. (2009) Insect-symbiont system: from complex relationships to biotechnological applications. Biotechnology Journal 4, 1753–1765.Google Scholar
Clark, E.L., Karley, A.J. & Hubbard, S.F. (2010) Insect endosymbionts: manipulation of insect herbivore trophic interactions? Protoplasma 244, 25–51.Google Scholar
Clausen, C.P. (1940) Entomophagous insects. New York, London, McGraw-Hill Book Company Inc., pp. 698.Google Scholar
Copello, A. (1922) Biología del moscardón cazador de abejas (Mallophora ruficauda Wiederman). Physis 6, 30–42.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.Google Scholar
Crespo, J.E. & Castelo, M.K. (2012) Barometric pressure influences host-orientation behavior in the larva of a diptera ectoparasitoid. Journal of Insect Physiology 58, 1562–1567.CrossRefGoogle ScholarPubMed
Crespo, J.E., Martínez, G.A. & Castelo, M.K. (2015) Exposure to competitors influences parasitism decisions in ectoparasitoid fly larvae. Animal Behaviour 100, 38–43.Google Scholar
Cruden, D.L. & Markovetz, A.J. (1987) Microbial ecology of the cockroach gut. Annual Review of Microbiology 41, 617–643.Google Scholar
Davis, T.S., Crippen, T.L., Hofstetter, R.W. & Tomberlin, J.K. (2013) Microbial volatile emissions as insect semiochemicals. Journal of Chemical Ecology 39, 840–859.Google 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.Google Scholar
Dennis, D.S., Barnes, J.K. & Knutson, L. (2013) Review and analysis of information on the biology and morphology of immature stages of robber flies (Diptera: Asilidae). Zootaxa 3673, 1–64.Google Scholar
Despland, E. & Hamzeh, S. (2004) Ontogenetic changes in social behavior in the forest tent caterpillar, Malacosoma disstria . Behavioral Ecology and Sociobiology 56, 177–184.Google 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.Google Scholar
Dicke, M. (1988) Microbial allelochemicals affecting the behavior of insects, mites, nematodes, and protozoa, in different trophic levels. pp. 125–163 in Barbosa, P. & Letourneau, , , D.K. (Eds) Letourneau Novel Aspects of Insect-Plant Interactions. Oxford, Wiley-Inter Science.Google Scholar
Dillon, R.J. & Dillon, V.M. (2004) The gut bacteria of insects: nonpathogenic interactions. Annual Reviews of Entomology 49, 71–92.Google Scholar
Dillon, R.J., Vennard, C.T. & Charnley, A.K. (2000) Exploitation of gut bacteria in the locust. Nature 403, 851.Google Scholar
Douglas, A.E. (1988) Experimental studies on the mycetome symbiosis in the leafhopper Euscelis incisus . Journal of Insect Physiology 34(11), 1043–1053.Google Scholar
Douglas, A.E. (1989) Mycetocyte symbiosis in insects. Biological Reviews 64, 409–434.Google Scholar
Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera . Annual Review of Entomology 43, 17–37.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
Farine, J-P., Cortot, J. & Ferveur, J-F. (2014) Drosophila adult and larval pheromones modulate larval food choice. Proceedings of Royal Society B Biological Science 281, 20140043.Google Scholar
Feener, D.H. Jr. & Brown, B.V. (1997) Diptera as parasitoids. Annual Review of Entomology 42, 73–97.Google Scholar
Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology 36, 533–543.Google Scholar
Flowers, R.W. & Costa, J.T. (2003) Larval communication and group foraging dynamics in the red-headed pine sawfly, Neodiprion lecontei (Fitch) (Hymenoptera: Symphyta: Diprionidae). Annals of the Entomological Society of America 96(3), 336–343.Google Scholar
Ganter, P.F. (2006) Yeast and invertebrate associations. pp. 303–370 in Rosa, C.A. & Gabor, P. (Eds) Biodiversity and Ecophysiology of Yeasts. Berlin, Springer-Verlag.Google Scholar
Godfray, H.C.J. (1994) Parasitoids. Behavior and Evolutionary Ecology. New Jersey, Princeton University Press, pp. 473.Google Scholar
Greenfield, M.D. (2002) Signallers and Receivers: Mechanisms and Evolution of Arthropod Communication. Oxford, Oxford University Press, pp. 414.Google Scholar
Groba, H.F. (2014) Caracterización morfológica de las larvas y de los receptores olfativos del parasitoide Mallophora ruficauda (Diptera: Asilidae) y determinación del origen de las claves químicas en el hospedador Cyclocephala signaticollis (Coleoptera: Scarabaeidae). PhD Thesis, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. http://digital.bl.fcen.uba.ar/Download/Tesis/Tesis_5497_Groba.pdf.Google Scholar
Groba, H.F. & Castelo, M.K. (2012) 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? Bulletin of Entomological Research 102, 315–323.Google Scholar
Grünwald, S., Pilhofer, M. & Höll, W. (2010) Microbial associations in gut systems of wood- and bark-inhabiting longhorned beetles (Coleoptera: Cerambycidae). Systematic and Applied Microbiology 33, 25–34.Google Scholar
Hoffmeister, T.S. & Gienapp, P. (1999) Exploitation of host's chemical communication in parasitoid searching for concealed host larvae. Ethology 105, 223–232.Google 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.Google Scholar
Huang, S-W. & Zhang, H-Y. (2013) The impact of environmental heterogeneity and life stage on the hindgut microbiota of Holotrichia parallela larvae (Coleoptera: Scarabaeidae). PLoS ONE 8(2), 14pp.Google Scholar
Huang, S-W., Zhang, H-Y., Marshall, S. & Jackson, T.A. (2010) The scarab gut: a potencial bioreactor for bio-fuel production. Insect Science 17, 175–183.Google Scholar
Hunt, D.W.A. & Borden, J.H. (1990) Conversion of verbenols to verbenone by yeast isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal of Chemical Ecology 16(4), 1385–1397.Google Scholar
Jumean, Z., Wood, C. & Gries, G. (2009) Frequency distribution of larval codling moth, Cydia pomonella L., aggregations on trees in unmanaged apple orchards of Pacific Northwest. Environmental Entomology 38(5), 1395–1399.Google Scholar
Klowden, M.J. (2007) Physiological Systems in Insects. London, Elsevier Academic Press, pp. 688.Google Scholar
Kühne, M., Ihnen, D., Möller, G. & Agthe, O. (2000) Stability of tetracycline in water and liquid manure. Journal of Veterinary Medicine A. Physiology, Pathology and Clinical Medicine 47(6), 379–384.Google Scholar
Leal, W.S. (1998) Chemical ecology of phytophagous scarab beetles. Annual Reviews of Entomology 43, 39–61.Google Scholar
Lemke, T., Stingl, U., Egert, M., Friederich, M.W. & Brune, A. (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva Pachnoda ephippiata (Coleoptera: Scarabaeidae). Applied and Environmental Microbiology 69(11), 6650–6658.Google Scholar
Leroy, P.D., Sabri, A., Verheggen, F.J., Francis, F., Thomart, P. & Haubruge, E. (2011) The semiochemically mediated interactions between bacteria and insects. Chemoecology 21, 113–122.Google Scholar
Lewis, W.J. & Martin, W.R. (1990) Semiochemicals for use with parasitoids: status and future. Journal of Chemical Ecology 16, 3067–3089.Google Scholar
Ma, P.W.K. & Ramaswamy, S.B. (2003) Biology and ultrastructure of sex pheromone-producing tissue. pp. 19–52 in Blomquist, G.J. & Vogt, R.G. (Eds) Biochemistry and Molecular Biology: the Biosynthesis and Detection of Pheromones and Plant Volatiles. London, Elsevier Academic Press.Google Scholar
Madden, J.L. (1968) Behavioural responses of parasites to the symbiotic fungus associated with Sirex noctilio F . Nature 218, 189–190.Google Scholar
Mathis, K.A., Philpott, S.M. & Moreira, R.F. (2011) Parasite lost: chemical and visual cues used by Pseudacteon in search of Azteca instabilis . Journal of Insect Behavior 24, 186–199.Google Scholar
Matthews, R.W. & Matthews, J.R. (2010) Insect Behavior. 2nd edn. Dordrecht, Heidelberg, London, New York, Springer Publishing, pp. 522.Google Scholar
Minard, G., Mavingui, P. & Moro, C.V. (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites & Vectors 6, 146.Google Scholar
Mitscher, L.A. (1978) The Chemistry of The Tetracycline Antibiotics. New York, Marcel Dekker Inc, pp. 352.Google Scholar
Moran, N.A., Plague, G.R., Sandström, J.P. & Wilcox, J.L. (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proceedings of the National Academy of Science of USA 100(2), 14543–14548.Google Scholar
Mota, T., Vitta, A.C.R., Lorenzo-Figueiras, A.N., Barezani, C.P., Zani, C.L., Lazzari, C.R., Diotaiuti, L., Jeffares, L., Bohman, B. & Lorenzo, M.G. (2014) A multi-species bait for Chagas disease vectors. PLoS Neglected Tropical Disease 8(2), e2677.Google Scholar
Oliver, K.M. & Martinez, A.J. (2014) How resident microbes modulate ecologically-important traits of insects. Current Opinion in Insect Science 4, 1–7.Google Scholar
Pettersson, E.M., Hallberg, E. & Birgersson, G. (2001) Evidence for the importance of odour-perception in the parasitoid Rhopalicus tutela (Walker) (Hym., Pteromalidae). Journal of Applied Entomology 125, 293–301.Google Scholar
Pochon, J. & Tardieux, P. (1965) Tecnicas de analisis en microbiologia del suelo. T.E.I. (Tecnica e Investigacion), Burgos, pp. 117.Google Scholar
Pontes, M., Smith, K., Smith, W. & Dale, C. (2009) Insect facultative symbionts: biology, culture, and genetic modification. pp. 377–395 in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis Volume 3. CRC Press, Boca Raton, London, New York, Washington, DC.Google Scholar
R Core Team (2015) R: A language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. http://www.R-project.org/.Google 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
Roitberg, B.D., Sircom, J., Roitberg, C.A., van Alphen, J.J.M. & Mangel, M. (1993) Life expectancy and reproduction. Nature 364, 108.Google Scholar
Rosner, B. (1995) Fundamentals of Biostatistics. Belmont, Duxbury Press, pp. 682.Google Scholar
Rutledge, C.E. (1996) A survey of identified kairomones and synomones used by insect parasitoids to locate and accept their hosts. Chemoecology 7, 121–131.Google Scholar
Sánchez Colin, M.deJ. (2004) Microbiología de suelos: técnicas, métodos y medio de cultivo. México D.F., Universidad Nacional Autónoma de México, pp. 52.Google Scholar
Sasaki, T. & Ishikawa, H. (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum . Journal of Insect Physiology 41(1), 41–46.Google Scholar
Singh, N. & Johnson, D.T. (2012) Attractiveness of an aggregation pheromone lure and chicken droppings to adults and larvae of Alphitobius diaperinus (Coleoptera: Tenebrionidae). Journal of Economic Entomology 105(6), 2196–2206.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.Google Scholar
Stireman, J.O. III, O'Hara, J.E. & Monty Wood, D. (2006) Tachinidae: evolution, behavior, and ecology. Annual Review of Entomology 51, 525–555.Google 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 States of America 92, 23–28.Google Scholar
Sullivan, B.T. & Berisford, C.W. (2004) Semiochemicals from fungal associates of bark beetle may mediate host location behavior or parasitoids. Journal of Chemical Ecology 30(4), 703–717.Google Scholar
Thompson, S.N. & Simpson, S.J. (2003) Nutrition. pp. 807–813 in Resh, V.H. & Cardé, R.T. (Eds) Encyclopedia of Insects. London, Elsevier Academic Press.Google Scholar
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.Google Scholar
Tsubaki, Y. & Shiotsu, Y. (1982) Group feeding as a strategy for exploiting food resources in the burnet moth Pryeria sinica . Oecologia 55, 12–20.Google 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.Google 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.Google 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.Google Scholar
Wertheim, B., Vet, L.E.M. & Dicke, M. (2003) Increased risk of parasitism as ecological costs of using aggregation pheromones: laboratory and field study of Drosophila – Leptopilina interaction. Oikos 100, 269–282.Google 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.Google Scholar
Wigglesworth, V.B. (1982) The Principles of Insect Physiology. New York, Springer Publishing, pp. 827.Google Scholar
Wiskerke, J.S.C., Dicke, M. & Vet, L.E.M. (1993) Larval parasitoiduses aggregation pheromone of adult hosts in foraging behavior: a solution to the reliability-detectability problem. Oecologia 93, 145–148.Google Scholar
Witzgall, P., Proffit, M., Rozpedowska, E., Becher, P.G., Andreadis, S., Coracini, M., Lindblom, T.U.T., Ream, L.J., Hagman, A., Bengtsson, M., Kurtzman, C.P., Piskur, J. & Knight, A. (2012) “This is not an apple” – Yeast mutualism in codling moth. Journal of Chemical Ecology 38, 949–957.Google Scholar
Wood, G.C. (1981) Asilidae. pp. 549–574 in McAlpine, J.F. (Eds) Manual of Neartic Diptera Volume 1. Ottawa, Department of Agriculture Research Branch.Google Scholar
Woolfolk, S.W., Cohen, A.C. & Inglis, G.D. (2004) Morphology of the alimentary canal of Chrysoperla rufilabris (Neuroptera: Crysopidae) adults in relation to microbial symbionts. Annals of the Entomological Society of America 97(4), 796–808.Google Scholar
Wyatt, T.D. (2003) Pheromones and Animal Behavior: Communication by Smell and Taste. Cambridge, Cambridge University Press, pp. 391.Google Scholar
Zar, J.H. (2010) Biostatistical Analisys. New Jersey, Pearson Prentice Hall International, pp. 663.Google Scholar
Zhang, H. & Jackson, T.A. (2008) Autochthonous bacterial flora indicated by PCR-DGGE of 16S rRNA gene fragments from the alimentary tract of Costelytra zealandica (Coleoptera: Scarabaeidae). Journal of Applied Microbiology 105, 1277–1285.Google Scholar
Zheng, W., Zhao, Y. & Zhang, H. (2012) Morphology and ultrastructure of the hindgut fermentation chamber of melolonthine beetle Holotrichia parallela (Coleoptera: Scarabaeidae) during larval development. Micron 43, 638–642.Google Scholar
Zuk, M. & Kolluru, G.R. (1998) Explotation of sexual signals by predators and parasitoids. The Quaterly Review of Biology 73(4), 415–438.CrossRefGoogle Scholar