Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T07:55:49.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Host specificity in the host-seeking larva of the dipteran parasitoid Mallophora ruficauda and the influence of age on parasitism decisions

Published online by Cambridge University Press:  19 February 2014

M.E. Barrantes  and
M.K. Castelo
M.E. Barrantes*
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 Güirales 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 Güirales 2160, Ciudad Universitaria, Pabellón II (C1428EHA), Ciudad de Buenos Aires, Argentina
*
*Author for correspondence Phone: (+54-11) 4576-3300. ext 214 Fax: (+54-11) 4576-3384 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Larvae of the robber fly Mallophora ruficauda are ectoparasitoids of white grubs and adults are an important apiculture pest in Argentina. Females oviposit on tall grasses and the second instar larva actively searches and locates hosts. There are nine potential hosts in the distribution area of this parasitoid and Cyclocephala signaticollis (Coleoptera: Scarabaeidae) is the most parasitized in the field. However, M. ruficauda has a certain degree of behavioural flexibility towards different host species, and not being a strict specialist. The conditions under which the parasitoid orientates and accepts different hosts’ species are unknown. We studied the host specificity of M. ruficauda towards three species of Cyclocephala genus and we determined whether this specificity depends on larval age. We also evaluated whether larva orientation towards Cyclocephala species changes with chemical cue concentration. We assessed host specificity measuring the orientation and acceptance behaviours towards kairomones extracts and live individuals of Cyclocephala species using M. ruficauda larvae of low and high life expectancy (i.e., young and aged second instar larvae). We observed that young larvae orientated only towards C. signaticollis chemical stimulus, whereas aged larvae orientated also towards C. modesta, and the same was observed with increasing stimuli's concentration. Both young and aged M. ruficauda larvae orientate towards live C. signaticollis and C. putrida species and rejected C. modesta. Also, we found that larvae accepted all Cyclocephala hosts. In conclusion, our results indicate that specificity in the laboratory, observed through host orientation and host acceptance behaviours, depends not only on the availability of host species, but also on the nature of the host's stimuli combined with parasitoid age.

Keywords

Asilidaehost locationlife expectancyScarabaeidae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 295 - 306
Copyright
Copyright © Cambridge University Press 2014 

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

Alvarado, L. (1980) Sistemática y bionomía de los estados inmaduros de coleópteros Scaraeibeidae que habitan en el suelo. Tesis doctoral, Facultad de Ciencias Naturales y Museo-UNLP, La Plata, Argentina.Google Scholar
Alvarado, L. (1983) Daños de insectos del suelo en semillas de plantas cultivadas. INTA Estación Experimental Regional Agropecuaria Pergamino, Informe Técnico n° 180: 7 pp. Trabajo presentado al IX Seminario Panamericano de semilla, Bs. As., 1980.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
Benelli, G., Gennari, G. & Canale, A. (2013 a) Host discrimination in the tephritid parasitoid Psyttalia concolor (Hymenoptera: Braconidae). Journal of Pest Science 86, 245–251.Google Scholar
Benelli, G., Revadi, S., Carpita, A., Giunti, G., Raspi, A., Anfora, G. & Canale, A. (2013 b) Behavioral and electrophysiological responses of the parasitic was Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) to Ceratitis capitata-induced fruit volatiles. Biological Control 64, 116–124.CrossRefGoogle Scholar
Benelli, G., Pacini, N., Conti, B. & Canale, A. (2013 c) Following a scented beetle: larval faeces as a key olfactory cue in host location of Stegobium paniceum (Coleoptera: Anobiidae) by Lariophagus distinguendus (Hymenoptera: Pteromalidae). Chemoecology 23, 129–136.Google Scholar
Bernstein, C. & Jervis, M. (2008) Food-searching in parasitoids: the dilemma of choosing between immediate or future fitness gains. pp. 129–171 in Wajnberg, E., Bernstein, C. & van Alphen, J.J.M. (Eds) Behavioral Ecology of Insects. Oxford, Blackwell Publishing Ltd.Google Scholar
Blaney, W.M., Schoonhoven, L.M. & Simmonds, M.S.J. (1986) Sensitivity variations in insect chemoreceptor: a review. Experientia 42, 13–19.Google Scholar
Brodeur, J. & Boivin, G. (2004) Functional ecology of immature parasitoids. Annual Review of Entomology 49, 27–49.CrossRefGoogle ScholarPubMed
Brodeur, J., Geervliet, B.E. & Vet, L.E.M. (1996) The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious parasitoid (Cotesia species). Entomologia Experimentalis et Applicata 81, 125–132.Google Scholar
Canale, A. & Benelli, G. (2012) Impact of mass-rearing on the host seeking behavior and parasitism by the fruit fly Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). Journal of Pest Science 85, 65–74.CrossRefGoogle Scholar
Castelo, M.K. & Capurro, A.F. (2000) Especificidad y denso-dependencia inversa en parasitoides con oviposición fuera del hospedador: el caso Mallophora ruficauda (Diptera: Asilidae) en la pampa argentina. Ecología Austral 10, 89–101.Google Scholar
Castelo, M.K. & Corley, J.C. (2004) Oviposition behaviour in the robber fly Mallophora ruficauda (Diptera: Asilidae). Annals of the Entomological Society of America 97(5), 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. & Crespo, J.E. (2012) Incidence of non-immunological defenses of soil white grubs on parasitism success of Mallophora ruficauda larva (Diptera: Asilidae). Insects 3, 692–708.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
Chapman, R.F. (1998) The Insects: Structure and Function. 4th edn. New York, Cambridge University Press.Google Scholar
Clark, C.W. & Mangel, M. (2000) Dynamic State Variable Models in Ecology: Methods and Applications. New York, Oxford University Press.Google Scholar
Colazza, S., Cusumano, A., Lo Giudice, D. & Peri, E. (2013) Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 2013, 1–17.Google Scholar
Cournoyer, M. & Boivin, G. (2004) Infochemical-mediated preference behavior of the parasitoid Microctonus hyperodae when searching for its adult weevil hosts. Entomologia Experimentalis et Applicata 112, 117–124.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. (2009) Insights to the host discrimination and host acceptance behaviour in a parasitoid (Diptera: Asilidae): implications for fitness. Journal of Insect Physiology 55, 1072–1078.Google Scholar
Crespo, J.E. & Castelo, M.K. (2010) Life history traits in a parasitoid dipteran species with free living and obligate parasitic immature stages. Physiological Entomology 35, 160–167.Google Scholar
Crespo, J.E. & Castelo, M.K. (2012) Barometric pressure influences host-orientation behavior in the larva of a dipteran ectoparasitoid. Journal of Insect Physiology 58, 1562–1567.Google Scholar
Crespo, J.E., Lazzari, C.R. & Castelo, M.K. (2011) Orientation mechanisms and sensory organs involved in host location in a dipteran parasitoid larva. Journal of Insect Physiology 57, 191–196.Google Scholar
Desneux, N., Barta, R.J., Hoelmer, K.A., Hopper, K.R. & Heimpel, G.E. (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160, 387–398.Google Scholar
Dicke, M. & Sabelis, M.W. (1988) Costs and benefits of chemical information conveyance: proximate and ultimate factors. Functional Ecology 2, 131–139.Google Scholar
Eggleton, P. & Belshaw, R. (1992) Insect parasitoids: an evolutionary overview. Philosophical Transactions of the Royal Society London B: Biological Sciences 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
Ellers, J., van Alphen, J.J.M. & Sevenster, J.G. (1998) A field study of size-fitness relationship in the parasitoid Asobara tabida . Journal of Animal Ecology 67, 318–324.Google Scholar
Feener, D.H. Jr. & Brown, B.V. (1997) Diptera as parasitoids. Annual Review of Entomology 42, 73–97.Google Scholar
Félix, A.-E., Calatayud, P.-A., Le Ru, B., Silvain, J.F. & Frérot, B. (2011) Sex pheromone composition and reproductive isolation in two Busseola species (Lepidoptera: Noctuidae) in Kenya. Chemoecology 2, 107–111.Google Scholar
Fischer, S., Samietz, J., Wäckers, F.L. & Dorn, S. (2001) Interaction of vibrational and visual cues in parasitoid host location. Journal of Comparative Physiology 187, 785–791.Google Scholar
Fletcher, J.P., Hughes, J.P. & Harvey, I.F. (1994) Life expectancy and egg load affect oviposition decisions of a solitary parasitoid. Proceedings of the Royal Society of London B 258, 163–167.Google Scholar
Flores-Prado, L. & Niemeyer, H.M. (2012) Host location by Ichneumonid parasitoids is associated with nest dimensions of the host bee species. Neotropical Entomology 41, 283–287.CrossRefGoogle ScholarPubMed
Futuyma, D.J. & Moreno, G. (1988) The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207–233.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavior and Evolutionary Ecology. Princeton, Princeton University Press.Google Scholar
Gray, D.A., Banuelos, C., Walker, S.E., Cade, W.H. & Zuk, M. (2007) Behavioral specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts. Animal Behavior 73, 99–104.Google Scholar
Greenfield, M.D. (2002) Signallers and Receivers: Mechanisms and Evolution of Arthropod Communication. Oxford, Oxford University Press.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
Guerrieri, F., Schubert, M., Sandoz, J.C. & Giurfa, M. (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biology 3(4), e60.Google Scholar
Hardy, I.C.W. (2002) Sex Ratios: Concepts and Research Methods. Cambridge, Cambridge University Press. Google Scholar
Heimpel, G.E., Neuhauser, C. & Hoogendoorn, M. (2003) Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecology Letters 6, 556–566.Google Scholar
Janssen, A. (1989) Optimal host selection by Drosophila parasitoids in the field. Functional Ecology 3, 469–479.Google Scholar
Javoiš, J. & Tammaru, T. (2004) Reproductive decisions are sensitive to cues of life expectancy: the case of a moth. Animal Behaviour 68, 249–255.Google Scholar
Javoiš, J. & Tammaru, T. (2006) The effect of egg load on readiness to accept a low-quality host plant is weak and age dependent in a geometrid moth. Ecological Entomology 31, 597–600.Google Scholar
Joyce, A.L., Millar, J.G., Gill, J.S., Singh, M., Tanner, D. & Paine, T.D. (2011) Do acoustic cues mediate host finding by Syngaster lepidus (Hymenoptera: Braconidae)? BioControl 56, 145–153.Google Scholar
Laumann, R.A., Blassioli Moraes, M.A., Čokl, A. & Borges, M. (2007) Eavesdropping on sexual vibratory signals of stink bugs (Hemiptera: Pentatomidae) by the egg parasitoid Telenomus podisi . Animal Behaviour 73, 637–649.Google 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.Google Scholar
Mangel, M. (1987) Oviposition site selection and clutch size in insects. Journal of Mathematical Biology 25, 1–22.Google Scholar
Mangel, M. & Clark, C.W. (1988) Dynamic Modelling in Behavioural Ecology. New Jersey, Princeton University Press.Google Scholar
Mohamed, S.A., Wharton, R.A., von Mérey, G. & Schulthess, F. (2006) Acceptance and suitability of different host stages of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and seven other tephritid fruit fly species to Tetrastichus giffardii Silvestri (Hymenoptera: Eulophidae). Biological Control 39, 262–271.Google Scholar
Morehead, S.A. & Feener, D.H. (2000) Visual and chemical cues used in host location and acceptance by a dipteran parasitoid. Journal of Insect Behavior 13, 613–625.Google Scholar
Potter, D.A. (1998) Destructive Turfgrass Insects: Biology, Diagnosis and Control. Chelsea, Ann Arbor Press.Google Scholar
Rabinovich, M. & Corley, J.C. (1997) An important new predator of honey bees. The robber fly Mallophora ruficauda Wiedemann (Diptera: Asilidae) in Argentina. American Bee Journal 137(4), 303–306.Google Scholar
Remedi de Gavotto, A.L. (1964) Ciclo biológico de Cyclocephala signaticollis Burm. (Coleoptera, Scarabaeidae) y caracteres específicos de su larva. INTA, Revista de Investigaciones Agropecuarias, Serie 5, 1(10), 151–161.Google Scholar
Roitberg, B. & Bernard, P. (2007) State dependent problems for parasitoids: case studies and solutions. pp. 337–356 in Wajnberg, E., Bernstein, C. & van Alphen, J.J.M. (Eds) Behavioral Ecology of Parasitoids. From Theoretical Approaches to Field Applications. Oxford, CAB International.Google Scholar
Roitberg, B.D., Mangel, M., Lalonde, R.G., Roitberg, C.A., van Alphen, J.J.M. & Vet, L. (1993) Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behavioral Ecology 3, 156–165.Google Scholar
Royer, L., Fournet, S. & Brunel, E. (1999) Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids. Oecologia 118, 59–68.Google Scholar
Ruther, J., Meiners, T. & Steidle, J.L.M. (2002) Rich in phenomena-lacking in terms: a classification of kairomones. Chemoecology 12, 161–167.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
Schmidt, J.M. & Smith, J.J.B. (1987 a) Measurement of host curvature by the parasitoid wasp Trichogramma minutum and its effects on host examination and progeny allocation. Journal of Experimental Biology 129, 151–164.CrossRefGoogle Scholar
Schmidt, J.M. & Smith, J.J.B. (1987 b) Short interval time measurement by a parasitoid wasp. Science 237, 903–905.Google Scholar
Sirot, E., Ploye, H. & Bernstein, C. (1997) State dependent superparasitism in a solitary parasitoid: egg load and survival. Behavioral Ecology 8, 226–232.Google Scholar
Slansky, F. Jr. (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. Journal of Insect Physiology 32, 255–261.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
Stephens, D.W. & Krebs, J.R. (1986) Foraging Theory (Monographs in Behavior and Ecology). Princeton, Princeton University Press.Google Scholar
Stireman, J.O. III, O'Hara, J.E. & Wood, D.M. (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
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
Torréns, J. (2013) A review of the biology of Eucharitidae (Hymenoptera: Chalcidoidea) from Argentina. Psyche: A Journal of Entomology 2013, 1–14.Google Scholar
Uefune, M., Kugimiya, S., Shimoda, T. & Takabayashi, J. (2013) Starvation and herbivore-induced plant volatiles affect the color preferences of parasitic wasps. BioControl 58, 187–193.Google Scholar
van Alphen, J.J.M. & Vet, L.E.M. (1986) An evolutionary approach to host finding and selection. pp. 23–61 in Waage, J.K. & Greathead, D. (Eds) Insect Parasitoids, 13th Symposium of the Royal Entomological Society of London. London, Academic Press.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
Vet, L.E.M., Hemerik, L., Visser, M.E. & Wäckers, F.L. (2002) Flexibility in host search and patch use strategies of insect parasitoids. pp. 39–64 in Lewis, E.E., Campbell, J.F. & Sukhdeo, M.V.K. (Eds) The Behavioural Ecology of Parasites. Oxon, CAB International.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
Wang, X.Y., Yang, Z.Q., Gould, J.R., Wu, H. & Ma, J.H. (2010) Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer. Biological Control 52, 24–29.Google Scholar
Wertheim, B. (2005) Evolutionary ecology of communication signals that induce aggregative behaviour. Oikos 109, 117–124.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
Yeates, D.K. & Greathead, D. (1997) The evolutionary pattern of host use in the Bombyliidae (Diptera): a diverse family of parasitoid flies. Biological Journal of the Linnean Society 60, 149–185.Google Scholar
Yong, T.H., Pitcher, S., Gardner, J. & Hoffmann, M.P. (2007) Odor specificity testing in the assessment of efficacy and non-target risk for Trichogramma ostriniae (Hymenoptera: Trichogrammatidae). Biocontrol Science and Technology 17, 135–153.Google Scholar
Zar, J.H. (2010) Biostatistical Analysis. 5th edn. Upper Saddle River, Prentice-Hall Inc.Google Scholar
Zuk, M. & Kolluru, G.R. (1998) Exploitation of sexual signals by predators and parasitoids. Quarterly Review of Biology 73, 415–438.Google Scholar