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Biological control of the stink bug Nezara viridula (Heteroptera: Pentatomidae) by two parasitoids and their interaction in non-crop habitats: a simulation model
Published online by Cambridge University Press: 21 December 2022
Abstract
Non-cultivated areas are resting, overwintering, feeding, and/or reproducing habitats for insects, and also places from where crop areas are colonized; thus, they are essential for understanding the biological control programs in agroecosystems. We developed a simulation model for a non-cultivated area of Buenos Aires province (Argentina), and we analyzed the control of Nezara viridula achieved by the action of two parasitoids: the oophagous Trissolcus basalis and the tachinid Trichopoda giacomellii, which attack older nymphs and adults. The model is a discrete time, deterministic, phenomenological, spatially homogeneous with a 1-week time interval simulation model, based on the age-structure and/or stage-structure of N. viridula and its two parasitoids. The host–parasitoid interactions were combined with a degree-day model affecting development times of T. giacomellii pupae and T. basalis pre-imaginal stages. The simultaneous attack of both parasitoid species enables the persistence of the system at low host densities, mediated by the functional response of the parasitoids, identified as population regulation factors. However, if only one parasitoid exists (i.e., only T. basalis or only T. giacomellii) the interaction N. viridula–parasitoid persisted but at higher density of N. viridula. These results explain the successful biological control of N. viridula after the introduction of T. basalis in the 1980s, when T. giacomellii was the only parasitoid present, unable to control N. viridula. Our model shows an indirect competition when both parasitoids are present: the attack of one of them diminished the potential number of hosts available to the other parasitoid species. In the field this interaction is obscured by the hibernation period which acted as a reset mechanism affecting the density and age/stage structure of all three populations. Our model was supported by field observations, and never exhibited the extinction of any of the parasitoids from the interaction.
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- Copyright © The Author(s), 2022. Published by Cambridge University Press
References
Aldrich, JR, Lusby, BE, Marron, GK, Nicolau, KC, Hoffman, MP and Wilson, LT (1989) Pheromone blends of green stink bug and possible parasitoid selection. Naturwissenschaften 76, 173–175.CrossRefGoogle Scholar
Antonino, P, La Porta, NC and Avalos, DS (1996) Importancia de las plantas hospederas en la dinámica poblacional de Nezara viridula (L.), plaga de soja. Agricientia 13, 13–23.Google Scholar
Barratt, BIP, Howarth, FG, Withers, TM, Kean, JM and Ridley, GS (2010) Progress in risk assessment for classical biological control. Biological Control 52, 245–254.CrossRefGoogle Scholar
Bercellini, N and Malacalza, L (1993) Plagas y sus depredadores en soja Glycine max (L.) en el noroeste de la provincia de Buenos Aires (Argentina). Turrialba 44, 244–254.Google Scholar
Bewick, S (2016) Current and future challenges of predicting insect population modelling. Functional Ecology 30, 128–129.CrossRefGoogle Scholar
Bewick, S, Cantrell, RS, Cosner, C and Fagan, WF (2016) Hoe resource phenology affect consumer population dynamics. The American Naturalist 187, 151–166.Google Scholar
Bianchi, FJJA, Booij, CJH and Tscharntke, T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society B 273, 1715–1727.CrossRefGoogle ScholarPubMed
Bimboni, H (1985) Control integrado de plagas en soja. En: Jornadas de Actualización Profesional, Instituto Nacional de Tecnología Agropecuaria, Agencia de Extensión Rural INTA Chivilcoy, Chivilcoy, 1985.Google Scholar
Catalán, J and Verdú Gallardo, MJ (2005) Evaluación de dos parasitoides de huevos de Nezara viridula. Boletín de Sanidad Vegetal Plagas 31, 187–198.Google Scholar
Cingolani, MF, Greco, N and Liljesthröm, G (2014) Egg parasitism of Piezodorus guildinii and Nezara viridula (Hemiptera: Pentatomidae) in soybean, alfalfa and red clover. Revista de Facultad de Agronomía de la UNCuyo 46, 15–27.Google Scholar
Clausen, CP (1978) Introduced parasites and predators of arthropod pests and weeds. A world review. Agriculture Handbook Nr 480. United States Department of Agriculture (USDA), Agricultural Research Service (ARS). Washington, DC, USA, 545 pp.Google Scholar
Cohen, JE, Bohk-Ewald, C and Rau, R (2018) Gompertz, Makeham, and Siler models explain Taylor's law in human mortality data. Demographic Research 38, 773–841.CrossRefGoogle Scholar
Colazza, S, Sucarino, A, Peri, E, Salerno, G, Conti, E and Bin, F (2004) Insect oviposition induces volatile emissions in herbaceous plants that attracts egg parasitoids. Journal of Experimental Biology 207, 47–53.CrossRefGoogle ScholarPubMed
Coombs, M (1997) Influence of adult food deprivation and body size on fecundity and longevity of Trichopoda giacomellii: a South American parasitoid of Nezara viridula. Biological Control 8, 119–123.CrossRefGoogle Scholar
Corrêa- Ferreira, BS (1993) Utilização do parasitóide Trissolcus basalis (Wollaston) no controle de percevejos da soja. Londrina, PR, Brazil, EMPRAPA.Google Scholar
Duelli, P and Obrist, MK (2003) Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic and Applied Ecology 4, 129–138.CrossRefGoogle Scholar
Fagan, WF, Bewick, S, Cantrell, S, Cosner, C, Varassin, IG and Inouye, DW (2014) Phenologically explicit models for studying plant–pollinators interaction under climate change. Theoretical Ecology 7, 289–197.CrossRefGoogle Scholar
Field, SA (1998) Patch exploitation, patch-leaving and pre-emptive patch defense in the parasitoid wasp Trissolcus basalis (Insecta: Scelionidae). Ethology 104, 323–338.CrossRefGoogle Scholar
Field, SA and Calbert, G (1998) Patch defense in the egg parasitoid Trissolcus basalis: when to begin fighting? Behaviour 135, 629–642.CrossRefGoogle Scholar
Field, SA, Keller, MA and Calbert, C (1997) The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defense. Ecological Entomology 22, 142–149.CrossRefGoogle Scholar
Gamundi, JC (1985) Manejo integrado de plagas en soja. Actas de las Primeras Jornadas sobre Manejo Integrado de Plagas. Santa Fe, Argentina.Google Scholar
Gard, B, Bout, A and Prisca, P (2022) Release strategies of Trissolcus basalis (Scelionidae) in protected crops against Nezara viridula (Pentatomidae): less is more. Crop Protection 161, 1–7.CrossRefGoogle Scholar
Harris, V and Todd, T (1980) Male mediate aggregation of males, females and fifth instar southern green stink bug, and concomitant attraction of a tachinid parasite: Trichopoda pennipes. Entomologia Experimentalis et Applicata 27, 117–146.CrossRefGoogle Scholar
Hasperué, W and Rabinovich, J (2014) GLIMSO: General Language to Integrate Modeling, Simulation and Optimization. A manual. Center for the Study of Parasites and Vectors, National University of La Plata, La Plata, Argentina. 9 pp. https://links.cepave.edu.ar/glimso-manual.Google Scholar
Hassell, MP (2000) Host–parasitoid population dynamics. Journal of Animal Ecology 69, 543–566.CrossRefGoogle Scholar
Hassell, MP and Varley, GC (1969) New inductive population model for insect parasites and its bearing in biological control. Nature 223, 1133–1137.CrossRefGoogle ScholarPubMed
Holland, J and Fahrig, L (2000) Effect of woody borders on insect density and diversity in crop fields: a landscape-scale analysis. Agriculture, Ecosystems & Environment 78, 115–122.CrossRefGoogle Scholar
Jervis, MA and Copland, MJW (1996) The life cycle. In Jervis, MA and Kidd, N (eds), Insect Natural Enemies: Practical Approaches to Their Study and Evaluation. London: Chapman & Hall, pp. 63–161.CrossRefGoogle Scholar
Jones, V (1995) Reassessment of the role of predators and Trissolcus basalis in biological control of the southern green stink bug, Nezara viridula (L) (Hemiptera: Pentatomidae) in Hawaii. Biological Control 5, 566–572.CrossRefGoogle Scholar
Jones, WA and Sullivan, MJ (1982) Role of host plants in population dynamics of sting bug pests of soybean in South Carolina. Environmental Entomology 11, 867–875.CrossRefGoogle Scholar
Jones, VP and Westcott, 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
Kiritani, K (1964) Natural control of populations of the southern green stink bug, Nezara viridula (L.). Researches in Population Ecology 6, 88–98.Google Scholar
Kiritani, K and Hokyo, N (1962) Studies on the life table on the southern green stink bug Nezara viridula. Journal of Applied Entomology and Zoology 6, 124–140.CrossRefGoogle Scholar
Kruess, A and Tscharntke, T (1994) Habitat fragmentation, species loss, and biological control. Science 264, 1581–1584.CrossRefGoogle ScholarPubMed
Landis, DA, Wratten, SD and Gurr, GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology 45, 175–201.CrossRefGoogle ScholarPubMed
La Porta, NC and Crouzel, IS (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
Liljesthröm, G (1992) Distribución de los ataques del parasitoide Trichopoda giacomellii (Diptera: Tachinidae) sobre una población de Nezara viridula (Hemiptera: Pentatomidae). Ecología Austral 2, 29–37.Google Scholar
Liljesthröm, G (1993) Superparasitismo y competencia intraespecífica entre larvas del parasitoide Trichopoda giacomellii (Blnchard) (Diptera: Tachinidae). Ecología Austral 3, 43–48.Google Scholar
Liljesthröm, G (1997) Persistencia de Trichopoda giacomellii (Diptera: Tachinidae) durante el período de inactividad invernal del huésped Nezara viridula (Hemiptera: Pentatomidae), en el nordeste de la provincia de Buenos Aires. Revista de la Sociedad Entomológica Argentina 56, 133–136.Google Scholar
Liljesthröm, GG and Avalos, DS (2015) Nuevas asociaciones entre Phasiinae (Díptera: Tachinidae) y Pentatomidae (Hemiptera: Heteroptera) fitófagos en la pampa ondulada (Argentina) y descripción del macho de dallasymia bosqi Blanchard. Revista de la Sociedad Entomológica Argentina 73, 145–152.Google Scholar
Liljesthröm, G and Bernstein, C (1990) Density dependence and regulation in the system Nezara viridula (L.) (Hemiptera: Pentatomidae), host and Trichopoda giacomellii (Blanchard) (Diptera: Tachinidae), parasitoid. Oecologia 84, 45–52.CrossRefGoogle Scholar
Liljesthröm, G and Coviella, C (1999) Aspectos de la dinámica poblacional de las chinches Nezara viridula y Piezodorus guildinii e implicancias e implicancias con relación a su manejo en el cultivo de soja. Revista de la Sociedad Entomológica Argentina 58, 141–149.Google Scholar
Liljesthröm, G and Rabinovich, J (2004) Modeling biological control: the population regulation of Nezara viridula by Trichopoda giacomellii. Ecological Applications 14, 254–267.CrossRefGoogle Scholar
Liljesthröm, G, Cingolani, MF and Rabinovich, JE (2013) The functional and numerical responses of Trissolcus basalis (Hymenoptera: Platygastridae) parasitizing Nezara viridula (Hemiptera: Pentatomidae) eggs in the field. Bulletin of Entomological Research 103, 441–450.CrossRefGoogle ScholarPubMed
Lin, HY and Myers, L (2006) Power and type I error rates of goodness-of-fit statistics for binomial generalized estimating equations (GEE) models. Computational Statistics & Data Analysis 50, 3432–3448.CrossRefGoogle Scholar
Luck, RF and Podoler, H (1985) Competitive exclusion of Aphytis lingnanensis by A. melinus: potential role of host size. Ecology 66, 904–913.CrossRefGoogle Scholar
Masoni, F and Frana, J (2008) Fluctuación poblacional del complejo de chinches en alfalfa. En Trumper, EV and Edelstein, JD (eds), Chinches Fitófagas en Soja. Revisión y Avances en el Estudio de su Ecología y Manejo. Manfredi: Ediciones INTA, pp. 89–96.Google Scholar
May, RM (1978) Host–parasitoid systems in patchy environments: a phenomenological model. Journal of Animal Ecology 47, 833–843.CrossRefGoogle Scholar
Meats, A and Castillo Pando, MS (2002) Ratio-dependent parasitism with Trissolcus basalis (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.CrossRefGoogle Scholar
Menge, BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecological Monographs 65, 21–74.CrossRefGoogle Scholar
Molinari, AM and Gamundi, JC (1993) Trichopoda giacomellii (Dipt.: Tachinidae) en poblaciones invernantes de Nezara viridula (Hemipt.: Pentatomidae). Revista Peruana de Entomologia 34, 50–52.Google Scholar
Morrison, WR III, Mathews, CR and Leskey, TC (2016) Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biological Control 97, 120–130.CrossRefGoogle Scholar
Murdoch, WW and Briggs, JC (1996) Theory for biological control: recent developments. Ecology 77, 2001–2013.CrossRefGoogle Scholar
Murdoch, WW, Briggs, JC and Nisbet, RM (1996) Competitive displacement and biological control in parasitoids: a model. The American Naturalist 148, 807–816.CrossRefGoogle Scholar
Nayak, PC, Rao, YR and Sudheer, KP (2006) Groundwater level forecasting in a shallow aquifer using artificial neural network approach. Water Resources Management 20, 77–90.CrossRefGoogle Scholar
Nicholson, AJ and Bailey, VA (1935) The balance of animal populations. Proceedings of the Zoological Society of London 3, 551–598.CrossRefGoogle Scholar
Olson, DM, Zeilinger, AR, Prescott, KK, Coffin, AW, Ruberson, JR and Andow, DA (2018) Landscape effects on Solenopsis invicta (Hymenoptera: Formicidae) and Geocoris spp. (Hemiptera: Geocoridae), two important omnivorous arthropod taxa in field crops. Environmental Entomology 47, 1057–1063.CrossRefGoogle ScholarPubMed
Panizzi, AR and Lucini, T (2016) What happened to Nezara viridula (L.) in the Americas. Possible reasons to explain population decline. Neotropical Entomology 45, 619–628.CrossRefGoogle Scholar
Panizzi, AR and Meneguim, AM (1989) Performance of nymphal and adult Nezara viridula on selected alternate host plants. Entomologia Experimentalis et Applicata 50, 215–223.CrossRefGoogle Scholar
Powell, JE and Shepard, BM (1982) Biology of Australian and United Status strains of Trissolcus basalis, a parasitoid of the green vegetable bug Nezara viridula. Austral Ecology 7, 181–186.CrossRefGoogle Scholar
Reitz, SR and Trumble, JT (2002) Competitive displacement among insects and arachnids. Annual Review of Entomology 47, 435–465.CrossRefGoogle ScholarPubMed
Roberts, A and Stone, L (2004) Advantageous indirect interactions in systems of competition. Journal of Theoretical Biology 228, 367–375.CrossRefGoogle ScholarPubMed
Seymour, JE and Sands, DPA (1993) Green vegetable bug (Nezara viridula (L)) (Hemiptera: Pentatomidae) in Australian pecans. In Corey, SA, Dall, DJ, Milne, WM (eds), Pest Control and Sustainable Agriculture. Canberra: Entomology, CSIRO Dic, pp. 223–225.Google Scholar
Strauss, SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends in Ecology & Evolution 6, 206–210.CrossRefGoogle ScholarPubMed
Tillman, G, Toewsb, M, Blaauwc, B, Sialc, A, Cottrelld, T, Talamase, E, Buntinf, D, Josephf, S, Balusug, R, Fadamirog, H, Lahirih, S and Patelc, D (2020) Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US. Biological Control 145, 1–13.CrossRefGoogle Scholar
Todd, JW (1989) Ecology and behavior of Nezara viridula. Annual Review of Entomology 34, 273–292.CrossRefGoogle Scholar
Tscharntke, T, Steffan-Dewenter, I, Kruess, A and Thies, C (2002) Characteristics of insect populations on habitat fragments: a mini review. Ecological Research 17, 229–239.CrossRefGoogle Scholar
Vicentini, R and Jiménez, HA (1977) El vaneo de los frutos en soja. INTA Serie Técnica, 47.Google Scholar
Witten, M and Satzer, W (1992) Gompertz survival model parameters: estimation and sensitivity. Applied Mathematics Letters 5, 7–12.CrossRefGoogle Scholar
Wootton, JT (1994) The nature and consequences of indirect effects in ecological communities. Annual Review of Ecological Systems 25, 443–466.CrossRefGoogle Scholar
Wright, MG and Diez, JM (2011) Egg parasitism by Trissolcus basalis (Hymenoptera: Scelionidae) in architecturally varied habitats, and observations on parasitism in Macadamia nut orchards and other habitats following augmentative release. Proceedings of the Hawaiian Entomological Society 43, 23–31.Google Scholar
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