Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T21:59:58.111Z Has data issue: false hasContentIssue false

Interactions between pupae of the pine processionary moth (Thaumetopoea pityocampa) and parasitoids in a Pinus forest

Published online by Cambridge University Press:  24 June 2015

C.P. Bonsignore*
Affiliation:
Laboratorio di Entomologia ed Ecologia Applicata – Dipartimento PAU, Università degli Studi Mediterranea di Reggio Calabria, Salita Melissari s.n, 89100 Reggio Calabria, Italy
F. Manti
Affiliation:
Laboratorio di Entomologia ed Ecologia Applicata – Dipartimento PAU, Università degli Studi Mediterranea di Reggio Calabria, Salita Melissari s.n, 89100 Reggio Calabria, Italy
E. Castiglione
Affiliation:
Laboratorio di Entomologia ed Ecologia Applicata – Dipartimento PAU, Università degli Studi Mediterranea di Reggio Calabria, Salita Melissari s.n, 89100 Reggio Calabria, Italy
*
*Author for correspondence Phone: +39 0965 1696318 Fax: +39 0965 385219 E-mail: [email protected]

Abstract

Parasitoids are significant enemies of many economically important insects and there is some evidence to suggest that their actions have a role in terminating the outbreaks of forest Lepidoptera populations. In this study, we examined the impact of parasitoids on the pupae of the pine processionary moth, and highlighted the presence of several parasitoid species for this developmental stage. A higher rate of parasitism was found when the pupal density in the soil was reduced, but the rate of parasitism was not influenced by pupal morphological traits or by the presence or absence of a cocoon around a pupa. Of the external factors examined, a delay in the time of descent of larvae from the trees had a positive effect on the level of parasitism. Observational data indicated that dipteran and hymenopteran were the most abundant parasitoids to emerge from moth pupae. Our study highlights the complexity of the parasitoid–host dynamics, and stresses the importance of carefully determining environmental effects on host–parasitoid relations.

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

REFERENCES

Avci, M. & Kara, K. (2002) Tachinidae parasitoids of Traumatocampa ıspartaensis from Turkey. Phytoparasitica 30, 361364.CrossRefGoogle Scholar
Barbaro, L. & Battisti, A. (2011) Birds as predators of the pine processionary moth (Lepidoptera: Notodontidae). Biological Control 6, 107114.CrossRefGoogle Scholar
Battisti, A., Bernardi, M. & Ghiraldo, C. (2000) Predation by the hoopoe (Upupa epops) on pupae of Thaumetopoea pityocampa and the likely influence on other natural enemies. BioControl 45, 311323.CrossRefGoogle Scholar
Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A. & Larsson, S. (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecological Applications 15, 20842096.CrossRefGoogle Scholar
Battisti, A., Stastny, M., Buffo, E. & Larsson, S. (2006) A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly. Global Change Biology 12, 662671.CrossRefGoogle Scholar
Battisti, A., Holm, G., Fagrell, B. & Larsson, S. (2011) Urticating hairs in Arthropods: their nature and medical significance. Annual Review of Entomology 56, 203220.Google ScholarPubMed
Berryman, A.A. (1996) What causes population cycles of forest Lepidoptera? Trends in Ecology and Evolution 11, 2832.Google ScholarPubMed
Biliotti, E. (1955) Vie endoparasitaire et diapause chez, Phryxe secunda caudata. B. B. Comptes Rendus Hebdomadaire des Sèances de l'Académie des Sciences 240, 915916.Google Scholar
Biliotti, E., Demolin, G. & Du Merle, P. (1967) Parasitisme de la Processionnaire du pin par Villa quinquefasciata Wied, apud Meig. (Dipt. Bombyliidae). Importance du comportement de ponte du parasite. Annales des Epiphyties 16, 279288.Google Scholar
Bonsignore, C.P. & Manti, F. (2013) Influence of habitat and climate on the flight of male pine processionary moths. Bulletin of Insectology 66, 2734.Google Scholar
Bonsignore, C.P., Manti, F., Castiglione, E. & Vacante, V. (2011) A study on the emergence sequence of pupal parasitoids of the pine processionary moth, Thaumetopoea pityocampa . Biocontrol Science and Technology 21, 587591.CrossRefGoogle Scholar
Boriani, M. (1994) Conomorium amplum (Walker, 1835): correct name of parasitoid from Hyphantria cunea (Drury, 1773) in Italy (Hymenoptera, Pteromalidae. Lepidoptera, Arctidae). Entomofauna 15, 431432.Google Scholar
Buxton, R.D. (1990) The influence of host tree species on timing of pupation of Thaumetopoea pityocampa Schiff. (Lep., Thaumetopoeidae) and its exposure to parasitism by Phryxe caudata Rond. (Dipt., Larvaevoridae). Journal of Applied Entomology 109, 302310.CrossRefGoogle Scholar
Corley, J.C. & Capurro, A.F. (2000) The persistence of simple host-parasitoid system with prolonged diapauses. Ecología Austral 10, 3745.Google Scholar
Devkota, B. & Schmidt, G.H. (1990) Larval development of Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae) from Greece as influenced by different host plants under laboratory conditions. Journal of Applied Entomology 109, 321330.CrossRefGoogle Scholar
Ducombs, G., Lamy, M., Mollard, S., Guillard, J.M. & Maleville, J. (1981) Contact dermatitis from processional pine caterpillar (Thaumetopoea pityocampa Den. and Schiff Lepidoptera). Contact Dermatitis 7, 287288.CrossRefGoogle Scholar
Du Merle, P. (1969) Existence de deux diapauses facultatives au cours du cycle biologique de Villa brunnea Beck. (Dipt., Bombyliidae). Comptes Rendus Hebdomadaire des Sèances de l'Académie des Sciences 268, 24332435.Google Scholar
Du Merle, P. (1979) Biologie de la larve planidium de Villa brunnea Beck., Diptère Bombyliide parasite de la processionnaire du pin. I. Rechereche et decouverte de l'hôte. Annales de Zoologie Ecologie Animale 11, 289304.Google Scholar
Du Merle, P. (1981) Biologie de la larve planidium de Villa brunnea [Dipt. Bombyliidae] parasite de la processionaire du pin. IV. Intensité des réactions siphonogänes de l'hôte. Annales De La Societe Entomologique De France 17, 191206.CrossRefGoogle Scholar
Elzinga, J.A., Zwakhals, K., Harvey, J.A. & Biere, A. (2007) The parasitoid complex associated with the herbivore Hadena bicruris (Lepidoptera: Noctuidae) on Silene latifolia (Caryophyllaceae) in the Netherlands. Journal of Natural History 41, 101123.CrossRefGoogle Scholar
Er, M.K., Tunaz, H. & Gökçe, A. (2007) Pathogenicity of entomopathogenic fungi to Thaumetopoea pityocampa (Schiff.) (Lepidoptera: Thaumatopoeidae) larvae in laboratory conditions. Journal of Pest Science 80, 235239.CrossRefGoogle Scholar
Federico, S., Avolio, E., Pasqualoni, L., De Leo, L., Sempreviva, A.M. & Bellecci, C. (2009) Preliminary results of a 30-year daily rainfall data base in southern Italy. Atmospheric Research 94, 641651.CrossRefGoogle Scholar
Gauthier, N., Dalleau-Clouet, C., Fargues, J. & Bon, M.C. (2007) Microsatellite variability in the entomopathogenic fungus Paecilomyces fumosoroseus: genetic diversity and population structure. Mycologia 99, 693704.CrossRefGoogle ScholarPubMed
Gerling, D. & Rejouan, N. (2004) Age-related pupal defenses against congeneric internecine activity in Encarsia species. Entomologia Experimentalis et Applicata 110, 8793.CrossRefGoogle Scholar
Godfray, H.C.J. & Shimada, M. (1999) Parasitoids as model organisms for ecologists. Researches on Population Ecology 41, 310.CrossRefGoogle Scholar
Hassell, M.P. (2000) Host–parasitoid population dynamics. Journal of Animal Ecology 69, 543566.CrossRefGoogle Scholar
Hatice, K., Ince, I.A., Kazim, S., Serife, I. & Zihni, D. (2009) Characterization of two Bacillus thuringiensis ssp. morrisoni strains isolated from Thaumetopoea pityocampa (Lep., Thaumetopoeidae). Biocontrol Science and Technology 19, 474485.Google Scholar
Hagen, S.B., Jepsen, J.U., Schott, T. & Ims, R.A. (2010) Spatially mismatched trophic dynamics: cyclically outbreaking geometrids and their larval parasitoids. Biology Letters 6, 566569.CrossRefGoogle ScholarPubMed
Hodar, J.A., Zamora, R. & Castro, J. (2002) Host utilisation by moth and larval survival of pine processionary caterpillar Thaumetopoea pityocampa in relation to food quality in three Pinus species. Ecological Entomology 27, 292301.CrossRefGoogle Scholar
Huchon, H. & Demolin, G. (1971) La bioécologie de la processionnaire du pin. Dispersion potentielle dispersion actuelle. Phytoma 23, 1120.Google Scholar
Ince, I.A., Hatice, K., Yilmaz, H., Demir, I. & Demirbaģ, Z. (2008) Isolation and identification of bacteria from Thaumetopoea pityocampa Den. and Schiff. (Lep., Thaumetopoeidae) and determination of their biocontrol potential. World Journal of Microbiology and Biotechnology 24, 30053015.CrossRefGoogle Scholar
Klemola, N., Kapari, L. & Klemola, T. (2008) Host plant quality and defence against parasitoids: no relationship between levels of parasitism and a geometrid defoliator immunoassay. Oikos 117, 926934.CrossRefGoogle Scholar
Klemola, N., Andersson, T., Ruohomaki, K. & Klemola, T. (2010) Experimental test of parasitism hypothesis for population cycles of a forest lepidopteran. Ecology 91, 25062513.CrossRefGoogle ScholarPubMed
Lamy, M. (1990) Contact dermatitis (Erucism) produced by processionary caterpillars (Genus Thaumetopoea). Journal of Applied Entomology 110, 425437.CrossRefGoogle Scholar
Lòpez-Sebastián, E., Tschorsning, H.P., Pujade–Villar, J., Guara, M. & Selfa, J. (2007) Sobre los parasitoides asociados a las fases de la larva y pupa de la procesionaria del pino en cuatro bosques meditteráneos (España). Bolletin de Sanidad Vegetal, Plagas 33, 5360.Google Scholar
Masutti, L., Battisti, A. (1990) Thaumetopoea pityocampa (Den. & Schiff.) in Italy – Bionomics and perspectives of integrated control. Journal of Applied Entomology 110, 229234.CrossRefGoogle Scholar
Jackson, M.A., McGuire, M.R., Lacey, L.A. & Wraigtht, S.P. (1997) Liquid culture production of desiccation tolerant blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus . Mycological Research 101, 3541.CrossRefGoogle Scholar
Pérez-Contreras, T. & Soler, J.J. (2004) Egg parasitoids select for large clutch sizes and covering layers in pine processionary moths (Thaumetopoea pityocampa). Annales Zoologici Fennici 41, 587597.Google Scholar
Pimentel, C., Calvão, T., Ferreira, C. & Nilsson, J.Å. (2010) Latitudinal gradients and the shaping of life-history traits in a gregarious caterpillar. Biological Journal of the Linnean Society 100, 224236.CrossRefGoogle Scholar
Ringel, M.S., Rees, M. & Godfray, H.C.J. (1998) The evolution of diapauses in a coupled host-parasitoid system. Journal of Theoretical Biology 194, 195204.CrossRefGoogle Scholar
Sanchez-Murillo, R.I., de la Torre-Martınez, M., Aguirre Linares, J. & Estrella, A.H. (2004) Light-regulated asexual reproduction in Paecilomyces fumosoroseus . Microbiology 150, 311319.CrossRefGoogle ScholarPubMed
Schmidt, G.H., Tanzen, E. & Bellin, S. (1999) Structure of egg-batches of Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae), egg parasitoids and rate of egg parasitism on the Iberian Peninsula. Journal of Applied Entomology 123, 449458.CrossRefGoogle Scholar
Schott, T., Hagen, S.B., Ims, R.A. & Yoccoz, N.G. (2010) Are population outbreaks in sub-arctic geometrids terminated by larval parasitoids? Journal of Animal Ecology 79, 701708.CrossRefGoogle ScholarPubMed
Stastny, M., Battisti, A., Petrucco Toffolo, E., Schlyter, F. & Larsson, S. (2006) Host plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa . Ecological Entomology 31, 481490.CrossRefGoogle Scholar
Tanhuanpää, M., Ruohomäki, K. & Kaitaniemi, P. (2003) Influence of adult and egg predation on reproductive successof Epirrita autumnata (Lepidoptera: Geometridae). Oikos 102, 263272.CrossRefGoogle Scholar
Tarasco, E. (1995) Morfologia larvale e biologia di Coelichneumon rudis (Boyer de Fonscolombe) (Hymenoptera: Ichneumonidae), endoparassitoide delle crisalidi della Thaumetopoea pityocampa (Denis et Schiffermüller) (Lepidoptera: Thaumetopoeidae). Entomologica, Bari 29, 551. (in Italian)Google Scholar
Triggiani, O. & Tarasco, E. (2002) Efficacy and persistence of entomopathogenic nematodes in controlling larval populations of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae). Biocontrol Science and Technology 12, 747752.CrossRefGoogle Scholar
Tsankov, G., Schmidt, G.H. & Mirchev, P. (1996) Parasitism of egg-batches of the pine processionary moth Thaumetopoea pityocampa (Den. & Schiff.) (Lep.,Thaumetopoeidae) in various regions of Bulgaria. Journal of Applied Entomology 120, 93105.CrossRefGoogle Scholar
Turchin, P., Wood, S.N., Ellner, S.P., Kendall, B.E., Murdoch, W.W., Fischlin, A., Casas, J., McCauley, E. & Briggs, C.J. (2003) Dynamical effects of plant quality and parasitism on population cycles of larch budmoth. Ecology 84, 12071214.CrossRefGoogle Scholar
Way, M.J., Paiva, M.R. & Cammell, M.E. (1999) Natural biological control of the pine processionary moth Thaumetopoea pityocampa (Den. & Schiff.) by the Argentine ant Linepithema humile (Mayr) in Portugal. Agricultural and Forest Meteorology 1, 2731.Google Scholar
Werno, J. & Lamy, M. (1994) Daily cycles for emission of urticating hairs from the pine processionary caterpillar (Thaumetopoea pityocampa S.) and the brown tail moth (Euproctis chrysorrhoea L.) (Lepidoptera) in laboratory conditions. Aerobiologia 10, 147151.CrossRefGoogle Scholar
Zhong-Qi, Y. & Baur, H. (2004) A new species of Conomorium Masi (Hyneboptera:Pteromalidae) parasitizing the Fall Webworm Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Bulletin de la Societe Entomologique Suisse 7, 213221.Google Scholar
Zwakhals, C.J. (2005) Pimpla processioneae and P. rufipes: specialist versus generalist Hymenoptera: Ichneumonidae, Pimplinae). Entomologische Berichten (Amsterdam) 65, 1416.Google Scholar