Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-17T12:40:18.974Z Has data issue: false hasContentIssue false

Penetration and encapsulation of the larval endoparasitoid Exorista larvarum (Diptera: Tachinidae) in the factitious host Galleria mellonella (Lepidoptera: Pyralidae)

Published online by Cambridge University Press:  20 December 2013

A. Valigurová*
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
V. Michalková
Affiliation:
Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, 845 06 Bratislava, Slovakia
P. Koník
Affiliation:
Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Biology Centre of the Academy of Sciences of the Czech Republic, Institute of Parasitology, Branišovská 31, 370 05 České Budějovice, Czech Republic
M.L. Dindo
Affiliation:
Dipartimento di Scienze e Tecnologie Agroambientali, Entomology Area, Università degli Studi di Bologna, Viale Fanin 42, 40127 Bologna, Italy
M. Gelnar
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
J. Vaňhara
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
*
*Author for correspondence Phone: +420 -549-49-7895 Fax: +420-541-211-214 E-mail: andreav@sci.muni.cz

Abstract

The tachinid fly Exorista larvarum (L.) (Diptera: Tachinidae) is a polyphagous larval endoparasitoid that deposits its eggs on the host exoskeleton of lepidopteran and tenthredinid larvae. The attachment of larval E. larvarum and the formation of the respiratory funnel were studied during infestation in the last larval instar of the wax moth, Galleria mellonella (L.) (Lepidoptera: Pyralidae). The tachinid larvae burrow through the host integument after hatching, using their robust cephalopharyngeal skeleton, leaving a dark spot at the point of their penetration as a result of host cuticle melanization. Endoparasitoid penetration induces the host cellular defence, resulting in the formation of a haemocyte capsule consisting of multi-cellular sheaths. This enveloping capsule later undergoes melanization, which is mostly obvious towards the posterior part of the endoparasitoid. The endoparasitoid uses the host encapsulation response to build a respiratory funnel from the modified host integument, leading to the host surface. The encapsulated larva remains attached to the respiratory funnel via an anal hook and cuticular spines until fully developed. Additional immunohistochemical analyses were used to study host–parasitoid interactions. Indirect immunofluorescence showed no labelling of potential tachinid antigens and confirmed no effect on the surrounding host tissues. A simulated parasitization with coated polybead microspheres revealed the mortal impact of tachinid antigens to the host. Hosts injected with antigen-coated polybeads died as a consequence of an acute and extensive immunological response to the tachinid antigens and not due to the trauma caused by foreign objects inside their body.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

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

Baerwald, R.J. (1979) Fine structure of hemocyte membranes and intercellular junctions formed during hemocyte encapsulation. pp. 155188 in Gupta, A.P. (Ed.) Insect Hemocytes. Cambridge, Cambridge University Press.Google Scholar
Baronio, P., Campadelli, G. & Gardenghi, G. (1974) Ricerche sulla formazione della guaina attorno alle larve dei Ditteri Larvevoridi. Bollettino dell'Istituto di Entomologia della Università di Bologna 32, 91103.Google Scholar
Belshaw, R. (1994) Life history characteristics of Tachinidae (Diptera) and their effect on polyphagy. pp. 145162 in Hawkins, B.A. & Sheehan, W. (Eds) Parasitoid Community Ecology. Oxford, UK, Oxford University Press.Google Scholar
Caron, V., Janmaat, A.F., Ericsson, J.D. & Myers, H.D. (2008) Avoidance of the host immune response by a generalist parasitoid, Compsilura concinnata Meigen. Ecological Entomology 33, 517522.Google Scholar
Depalo, L. (2009) Efficacia del parassitoide Exorista larvarum (L.) (Diptera Tachinidae) prodotto in cattività: miglioramento delle tecniche di allevamento, accettabilità di insetti bersaglio e ruolo svolto dalla pianta sul processo di parassitizzazione. Dissertation, Università di Bologna.Google Scholar
Dindo, M.L. (2011) Tachinid parasitoids: are they to be considered as koinobionts? BioControl 56, 249255.Google Scholar
Dindo, M.L., Farneti, R., Scapolatempo, M. & Gardenghi, G. (1999) In vitro rearing of the parasitoid Exorista larvarum (L.) (Diptera: Tachinidae) on meat homogenate-based diets. Biological Control 16, 258266.CrossRefGoogle Scholar
Eggleton, P. & Belshaw, R. (1993) Comparisons of dipteran, hymenopteran and coleopteran parasitoids: provisional phylogenetic explanations. Biological Journal of the Linnean Society 48, 213226.Google Scholar
Feener, D.H. & Brown, B.V. (1997) Diptera as parasitoids. Annual Review of Entomology 42, 7397.CrossRefGoogle ScholarPubMed
Gardenghi, G. & Mellini, E. (1995) Note sul canale alimentare delle larve del parassitoide Exorista larvarum (L.) (Dipt. Tachinidae). Bollettino dell'Istituto di Entomologia “Guido Grandi” University of Bologna 49, 197209.Google Scholar
Hafez, M. (1953 a) Studies on Tachina larvarum L. (Diptera, Tachinidae) I. Preliminary notes. Bulletin de la Société Fouad Ier d'Entomologie 37, 255266.Google Scholar
Hafez, M. (1953 b) Studies on Tachina larvarum L. (Diptera, Tachinidae) II. Morphology of the adult and of its early stages. Bulletin de la Société Fouad Ier d'Entomologie 37, 267304.Google Scholar
Hafez, M. (1953 c) Studies on Tachina larvarum L. (Diptera, Tachinidae) III. Biology and life-history. Bulletin de la Société Fouad Ier d'Entomologie 37, 305335.Google Scholar
Humason, G.L. (1967) Animal Tissue Techniques. 2nd edn. San Francisco and London, W.H. Freeman and Company.Google Scholar
Ichiki, R. & Shima, H. (2003) Immature life of Compsilura concinnata (Meigen) (Diptera: Tachinidae). Annals of the Entomological Society of America 96, 161167.CrossRefGoogle Scholar
Kathirithamby, J., Ross, L.D. & Johnston, J.S. (2003) Masquerading as self? Endoparasitic Strepsiptera (Insecta) enclose themselves in host-derived epidermal bag. Proceedings of the National Academy of Sciences U.S.A. 100, 76557659.Google Scholar
Mellini, E. (1991) Sinossi di biologia dei Ditteri Larvevoridi (Studi sui Ditteri Larvevoridi. L contributo). Bollettino dell'Istituto di Entomologia “Guido Grandi” dell'Università di Bologna 45, 138.Google Scholar
Mellini, E. & Cucchi, C. (1965) Origine e struttura dell'imbuto respiratorio indotto da Steiniella callida Meig. (Dipt. Larvaevoridae) nelle larve di Melasoma populi L. (Col. Chrysomelidae). Bollettino dell'Istituto di Entomologia della Università di Bologna 27, 215227.Google Scholar
Michalková, V., Valigurová, A., Dindo, M.L. & Vaňhara, J. (2009) Larval morphology and anatomy of the parasitoid Exorista larvarum (Diptera: Tachinidae), with an emphasis on cephalopharyngeal skeleton and digestive tract. Journal of Parasitology 95, 544554.CrossRefGoogle ScholarPubMed
Pennacchio, F. & Strand, M.R. (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annual Review of Entomology 51, 233258.Google Scholar
Ratner, S. & Vinson, S.B. (1983) Phagocytosis and encapsulation: cellular immune response in Arthropoda. American Zoologist 23, 185194.CrossRefGoogle Scholar
Rizki, R.M. & Rizki, T.M. (1990) Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophila melanogaster . Journal of Insect Physiology 36, 523529.Google Scholar
Salt, G. (1968) The resistance of insect parasitoids to the defence reactions of their hosts. Biological Reviews of the Cambridge Philosophical Society 43, 200232.Google Scholar
Salt, G. (1970) The Cellular Defence Reactions of Insects. Cambridge Monographs in Experimental Biology. Great Britain, Cambridge University Press.CrossRefGoogle Scholar
Schmit, A.R. & Ratcliffe, N.A. (1977) The encapsulation of foreign tissue implants in Galleria mellonella larvae. Journal of Insect Physiology 23, 175184.Google Scholar
Stireman, J.O. III, O'Hara, J.E. & Wood, D.M. (2006) Behavior, ecology and evolution of tachinid parasitoids. Annual Review of Entomology 51, 525555.Google Scholar
Strand, M.R. & Pech, L.L. (1995) Immunological basis for compatibility in parasitoid–host relationships. Annual Review of Entomology 40, 3156.Google Scholar
Van den Bosch, R. (1964) Encapsulation of the eggs of Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) in larvae of Hypera brunneipennis (Boheman) and Hypera postica (Gyllenhal) (Coleoptera: Curculionidae). Journal of Insect Pathology 6, 343367.Google Scholar
Vinson, S.B. (1990) How parasitoids deal with the immune system of their host: an overview. Archives of Insect Biochemistry and Physiology 13, 327.CrossRefGoogle Scholar