Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-07-03T06:18:15.392Z Has data issue: false hasContentIssue false
  • English
  • Français

The functional and numerical responses of Trissolcus basalis (Hymenoptera: Platygastridae) parasitizing Nezara viridula (Hemiptera: Pentatomidae) eggs in the field

Published online by Cambridge University Press:  18 March 2013

G.G. Liljesthröm ,
M.F. Cingolani  and
J.E. Rabinovich
G.G. Liljesthröm*
Affiliation:
Laboratory of Pest Ecology, CEPAVE (CONICET CCT La Plata – UNLP), Calle 2 # 584, La Plata (B1902CHX), Buenos Aires, Argentina
M.F. Cingolani
Affiliation:
Laboratory of Pest Ecology, CEPAVE (CONICET CCT La Plata – UNLP), Calle 2 # 584, La Plata (B1902CHX), Buenos Aires, Argentina
J.E. Rabinovich
Affiliation:
Laboratory of Pest Ecology, CEPAVE (CONICET CCT La Plata – UNLP), Calle 2 # 584, La Plata (B1902CHX), Buenos Aires, Argentina
*
*Author for correspondence Phone: +54 221 4233471 Fax: +54 221 4232327 E-mail: gerardo@cepave.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

Trissolcus basalis has been used as a biological control agent of its main host, Nezara viridula, in many countries. However, estimations of its functional and numerical responses in the field are lacking. We estimated the density of N. viridula eggs, the proportion of parasitized N. viridula eggs, and the number of T. basalis adults/trap in the field. We transformed relative parasitoid density to an absolute density, and estimated the parasitoid's attack rate, a, and the mutual interference parameter, m, in two ways: following Arditi & Akçakaya (1990) and using the Holling–Hassell–Varley model with two iterative techniques. The attack rate estimated by both methods were a=1.097 and a=0.767, respectively. Parameter m varied less between methods: m=0.563 and m=0.586, respectively, and when used to calculate the number of parasitized N. viridula eggs per m2, differences with the observed values were not significant. The numerical response of T. basalis was affected by the sex allocation of their progeny and the proportion of adult parasitoids trapped decreased with field parasitoid population density. Theoretical models show that 0<m<1 is a stabilizing factor and previous re-analysis of field data showed a mean m value of 0.8. The Holling–Hassell–Varley model leads to a flexible description of the functional response allowing to predict acceptable weekly host parasitism. The pre-imaginal parasitoid survival and the change in sex ratio as a function of parasitoid density adequately describe the numerical functional response of the parasitoid.

Keywords

Trissolcus basalisparasitoidNezara viridulahostfunctional responsenumerical responsecoefficient of interferencepre-adult survivorshipsex ratio
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 4 , August 2013 , pp. 441 - 450
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

Abrams, P.A. & Ginzburg, L.R. (2000) The nature of predation: prey dependent, ratio dependent or neither? Trends in Ecology and Evolution 15, 337–341.Google Scholar
Arditi, R. & Akçakaya, H.R. (1990) Underestimation of mutual interference of predators. Oecologia 83, 358–361.Google Scholar
Arditi, R. & Ginzburg, L.R. (1989) Coupling in predator–prey dynamics: ratio dependence. Journal of Theoretical Biology 139, 311–326.Google Scholar
Arnold, C.Y. (1959) The determination and significance of the base temperature in a linear heat unit system. American Society of Horticultural Science 4, 431–445.Google Scholar
Beddington, J.R. (1975) Mutual interference between parasites or predators and its effect on searching efficiency. Journal of Animal Ecology 44, 331–340.Google Scholar
Canto-Silva, C.R., Kolberg, R., Romanowski, H.P. & Redaelli, L.R. (2006) Dispersal of the egg parasitoid Gryon gallardoi (Brethes) (Hymenoptera: Scelionidae) in tobacco crops. Brazilian Journal of Biology 66, 9–17.Google Scholar
Catalán, J. & Verdú Gallardo, M.J. (2005) Evaluación de dos parasitoides de huevos de Nezara viridula. Boletín de Sanidad Vegetal Plagas 31, 187–198.Google Scholar
Cave, R.D. & Gaylor, M.J. (1989) Functional response of Telenomus reynoldsi [Hym.: Scelionidae] at five constant temperatures and in an artificial plant arena. BioControl 34, 3–10.Google Scholar
Corrêa-Ferreira, B.S. (1993) Utilização do parasitóide Trissolcus basalis (Wollaston) no controle de percevejos da soja. Londrina, PR, Brazil, Embrapa.Google Scholar
Corrêa-Ferreira, B.S. & Moscardi, F. (1995) Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biological Control 5, 196–202.Google Scholar
Dauphin, G.P., Coquillard, S., Colazza, S., Peri, E. & Wajnberg, E. (2009) Host kairomone learning and foraging success in an egg parasitoid: a simulation model. Ecological Entomology 34, 193–203.Google Scholar
DeAngelis, D.L., Goldstein, R.A. & O'Neill, R.V. (1975) A model for trophic interaction. Ecology 56, 881–892.Google Scholar
DeLong, J.P. & Vasseur, D.A. (2011) Mutual interference is common and mostly intermediate in magnitude. BioMed Central Ecology 11, 1–8.Google Scholar
Doetzer, A.K. & Foerster, L.A. (2007) Desenvolvimento, longevidade e reprodução de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em condições naturais durante a entressafra da soja no sul do Paraná. Neotropical Entomology 36, 233–242.Google Scholar
Driessen, G. & Hemerik, L. (1992) The time and egg budget of Leptopilina clavipes, a parasitoid of larval Drosophila. Ecological Entomology 17, 17–27.Google Scholar
Field, S.A. (1998) Patch exploitation, patch-leaving and pre-emptive patch defense in the parasitoid wasp Tirssolcus basalis (Insecta: Scelionidae). Ethology 104, 323–338.CrossRefGoogle Scholar
Field, S.A. & Calbert, G. (1998) Patch defence in the egg parasitoid Trissolcus basalis: when to begin fighting? Behaviour 135, 629–642.CrossRefGoogle Scholar
Field, S.A. & Calbert, G. (1999) Don't count your eggs before they're parasitized: contest resolution and the trade-offs during patch defense in a parasitoid wasp. Behavioral Ecology 10, 122–127.Google Scholar
Field, S.A., Keller, M.A. & Calbert, G. (1997) The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence. Ecological Entomology 22, 142–149.Google Scholar
Field, S.A., Keller, M.A. & Austin, A.D. (1998) Field ecology and behaviour of the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae). Transactions of the Royal Society of South Australia 122, 65–71.Google Scholar
Fox, L.R., Letourneau, D.K., Eisenbach, J., & Van Nouhuys, S. (1990) Parasitism rates and sex ratios of a parasitic wasp: effect of herbivore and plant quality. Oecologia 83, 414–419.Google Scholar
Free, C.A., Beddington, J.R. & Lawton, J.H. (1977) On the inadequacy of simple models of mutual interference for parasitism and predation. Journal of Animal Ecology 46, 543–554.Google Scholar
Ginzburg, L.R. & Jensen, C.X. (2008) From controversy to consensus: the indirect interference functional response. Verhandlungen des Internationalen Verein Limnologie 30, 297–301.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ.Google Scholar
Godfray, H.C.J. & Pacala, S.W. (1992) Aggregation and the population dynamics of parasitoids and predators. American Naturalist 140, 30–40.Google Scholar
Godin, C. & Boivin, G. (2000) Effects of host age on parasitism and progeny allocation in Trichogrammatidae. Entomologia Experimentalis et Applicata 97, 149–160.Google Scholar
Haefner, J.W. (1996) Modelling Biological Systems. Principles and Applications. Chapman & Hall, New York.CrossRefGoogle Scholar
Hamilton, G.C. (1967) Extraordinary sex ratios. Science 156, 477–488.Google Scholar
Hassell, M.P. (1971) Mutual interference between searching insect parasites. Journal of Animal Ecology 40, 473–486.CrossRefGoogle Scholar
Hassell, M.P. (1978) The Dynamics of Arthropod Predator–Prey Systems. Princeton University Press, Princeton, NJ, USA.Google Scholar
Hassell, M.P. (2000) Host-parasitoid population dynamics. Journal of Animal Ecology 69, 543–566.Google Scholar
Hassell, M.P. & May, R.M. (1973) Stability in insect host-parasite models. Journal of Animal Ecology 42, 693–726.Google Scholar
Hassell, M.P. & Varley, G.C. (1969) New inductive population model for insect parasites and its bearing in biological control. Nature 223, 1133–1137.Google Scholar
Hassell, M.P., Waage, J.K. & May, R.M. (1983) Variable parasitoid sex ratios and their effect on host–parasitoid dynamics. Journal of Animal Ecology 52, 889–904.Google Scholar
Heads, P.A. & Lawton, J.H. (1983) Studies on the natural enemy complex of the holly leaf-miner: the effects of scale on the detection of aggregative responses and the implication for biological control. Oikos 40, 267–276.Google Scholar
Holling, C.S. (1959) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Canadian Entomologist 91, 293–320.Google Scholar
Jervis, M.A. & Copland, M.J.W. (1996) The life cycle. pp. 63–161in Jervis, M.A. & Kidd, N. (Eds) Insect natural enemies: practical approaches to their study and evaluation. London, Chapman & Hall.Google Scholar
Jervis, M.A., Heimpel, G.E., Ferns, P.N., Harvey, J.A. & Kidd, N.A.C. (2001) Life-history strategies in parasitoid wasps: a comparative analysis of “ovigeny”. Journal of Animal Ecology 70, 442–458.Google Scholar
Jones, V.P. & Westcot, P. (2002) The effect of seasonal changes on Nezara viridula (L.) (Hemiptera: Pentatomidae) and Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in Hawaii. Biological Control 23, 115–120.CrossRefGoogle Scholar
La Porta, N.C. & Crouzel, I.S. (1984) Estudios básicos para el control biológico de Nezara viridula (L., 1758) (Hemiptera: Pentatomidae) en la Argentina. Revista de la Sociedad Entomológica Argentina 43, 119–143.Google Scholar
Laumann, R.A., Moraes, M.C.B., Pareja, M., Alarcao, G.C., Botelho, A.C., Maia, A.H.N., Leonardecz, E. & Borges, M. (2008) Comparative biology and functional response of Trissolcus spp. (Hymenoptera: Scelionidae) and implications for stink bugs (Hemiptera: Pentatomidae) biological control. Biological Control 44, 32–41.Google Scholar
Liljesthröm, G. & Bernstein, C. (1990) Density dependence and regulation in the system Nezara viridula (L.) (Hemiptera: Pentatomiade), host and Trichopoda giacomellii (Blanchard) (Diptera:Tachinidae), parasitoid. Oecologia 84, 45–52.Google Scholar
Liljesthröm, G. & Cameán, P. (1992) Parasitismo de una población de la “chinche verde” Nezara viridula (L.) (Hemiptera: Pentatomidae) por el parasitoide oófago Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae). Revista de la Facultad de Agronomía, La Plata 68, 71–76.Google Scholar
Liljesthröm, G. & Rabinovich, J.E. (2004) Modeling biological control: the population regulation of Nezara viridula by Trichopoda giacomellii. Ecological Applications 14, 254–267.Google Scholar
Liljesthröm, G.G. (1983) Algunos aspectos de la demografía de Nezara viridula (L.) (Hemiptera: Pentatomidae) en condiciones de laboratorio. Revista de la Sociedad Entomológica Argentina 42, 383–396.Google Scholar
Loch, A.D. (2000) Abundance, distribution, and availability of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) hosts in a soybean agricultural system in southeastern Queensland. Biological Control 18, 120–135.Google Scholar
Mangel, M. (1989) An evolutionary interpretation of the “motivation to oviposit”. Journal of Evolutionary Biology 2, 157–172.Google Scholar
Meats, A. & Castillo Pando, M.S. (2002) Ratio-dependent parasitism with Tirssolcus basalis (Wollaston) (Hymenoptera: Scelionidae) on eggs rafts of Nezara viridula (Linnaeus) (Hemiptera: Pentatomidae): effect of experimental variables and compatibility of “ratio” and “Holling” models. Australian Journal of Entomology 41, 243–252.Google Scholar
Nicholson, A.J. & Bailey, V.A. (1935) The balance of animal populations. Proceedings of the Zoological Society of London 3, 551–598.Google Scholar
Powell, J.E. & Shepard, B.M. (1982) Biology of Australian and United States strains of Trissolcus basalis, a parasitoid of the green vegetable bug Nezara viridula. Austral Ecology 7, 181–186.CrossRefGoogle Scholar
Quicke, D.L.J. (1997) Parasitic wasps. Chapman & Hall. London, UK.Google Scholar
Roitberg, B.D., Mangel, M., Lalonde, R.G., Roitberg, C.A., van Alphen, J.J.M. & Vet, L.E.M. (1992) Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behavioral Ecology 3, 156–165.Google Scholar
Rosi, M.C., Isidoro, N., Colazza, S. & Bin, F. (2001) Source of the host marking pheromone in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Journal of Insect Physiology 47, 989–995.Google Scholar
Royama, T. (1971) A comparative study of models for predation and parasitism. Researches on Population Ecology S1, 1–91.Google Scholar
Snedecor, G.W. & Cochran, W.G. (1980) Statistical Methods. Iowa State University Press, Ames, Iowa, USA.Google Scholar
Solomon, M.E. (1949) The natural control of animal population. Journal of Animal Ecology 18, 1–35.Google Scholar
Sujii, E.R., Costa, M.L.M., Pires, C.S., Colazza, S. & Borges, M. (2002) Inter- and intra-guild interactions in egg parasitoid species of the soybean stink bug complex. Pesquisa Agropecuária Brasileira 37, 1541–1549.Google Scholar
van Alphen, J.J.M. & Visser, M.E. (1990) Superparasitism as an adaptative strategy for insect parasitoids. Annual Review of Entomology 35, 59–79.Google Scholar
van der Hoeven, N. & Hemerik, L. (1990) Superparasitism as an ESS: to reject or not to reject, that is the question. Journal of Theoretical Biology 146, 467–482.CrossRefGoogle ScholarPubMed
Villemereuil, P.B. de & López-Sepulcre, A. (2011) Consumer functional responses Ander intra and inter-specific interference competition. Ecological modelling 222, 419–426.Google Scholar
Wajnberg, E. (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioural mechanisms. Behavioural Ecology and Sociobiology 60, 589–611.Google Scholar
Watt, K.E.P. (1959) A mathematical model for the effect of densities of attacked and attacking species on the number attacked. Canadian Entomologist 91, 129–144.Google Scholar
Weisser, W.W. & Houston, A.I. (1993) Host discrimination in parasitic wasps: when it is advantageous? Functional Ecology 7, 27–39.Google Scholar
Wilson, F. (1961) Adult reproductive behaviour in Asolcus basalis (Hymenoptera: Scelionidae). Australian Journal of Zoology 9, 737–751.CrossRefGoogle Scholar