Predation response of Nabis pseudoferus (Hemiptera: Nabidae) on untreated and Metarhizium anisopliae-treated larvae of Tuta absoluta (Lepidoptera: Gelechidae)

Volume 8, Issue 3
June 2019
Pages 311-322

Document Type : Original Research

Authors

1 Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran.

2 Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, Iran.

Abstract
Functional response is an important behavioral characteristic of prey-predator interactions that can be utilized for assessing impact of natural enemies. In this research, the functional response of Nabis pseudoferus Remane females was examined to the third-instar larvae of Tuta absoluta (Meyrick) which were exposed to LC30 (2.03 × 104 conidia/ml) values of Metarhizium anisopliae (Metschnikoff) Sorokin isolate DEMI 001. Six densities of the prey (1, 2, 4, 8, 10 and 16) were exposed to the predator (0, 24, 48 and 72 h) after inoculation. N. pseudoferus exhibited a type II functional response to prey density in all treatments, indicating that predation increases asymptotically to a satiation level. The highest and the lowest attack rates (a) were 0.1052 ± 0.0440 and 0.0509 ± 0.0133h-1 for 48h and 72h post-infection treatments, respectively. Maximum theoretical predation rate (T/Th) was estimated 10.96 in control. Our results suggest that M. anisopliae and N. pseudoferus, can be a useful combination in pest management of tomato leaf miner, although it must be confirmed in field condition.


Keywords

Agboton, B. V., Hanna, R., Onzo, A., Vidal, S. and von Tiedemann, A. 2013. Interactions between the predatory mite Typhlodromalus aripo and the entomopathogenic fungus Neozygites tanajoae and consequences for the suppression of their shared prey/host Mononychellus tanajoa. Experimental and Applied Acarology. 60: 205-217.
Alma, C. R., Goettel, M. S., Roitberg, B. D. and Gillespie, D. 2007. Combined effects of the entomophatogenic fungus Paecilomyces fumosoroseus Apoka-97 and the generalist predator Dicyphus hesperus on whitefly populations. BioControl. 52: 669-681.
Arbab, A., Heydari, N. and Pakyari, H. 2016. Temperature-dependent development of pale damsel bug, Nabis capsiformis Geramer (hemiptera: nabidae) using linear and non-linear models. Crop Protection. 89: 248-254.
Baniameri, V., and Cheraghian, A. 2012. The first report and control strategies of Tuta absoluta in Iran. EPPO Bulletin. 42: 322–324.
Barlow, N. D. and Goldson, S. L. 1993. A modelling analysis of the successful biological control of Sitona discoideus (Coleoptera: Curculionidae) by Microctonus aethiopoides (Hymenoptera: Braconidae) in New Zealand. Journal of Applied Ecology. 30: 165–178.
Barrientos, Z. R., Apablaza, H. J., Norero, S. A. and Estay, P. P. 1998. Threshold temperature and thermal constant for development of the South American tomato moth, Tuta absoluta (Lepidoptera, Gelechiidae). Ciencia Investigacion Agraria. 25: 133-137.
Biondi, A., Guedes, R. N. C., Wan, F. H., Desneux, D. 2018. Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future. Annual Review of Entomology. 63: 239-258.
Cabello, T., Gallego, J. R., Fern´andez-Maldonado, F. J., Soler, A., Beltran, D, Parra, A. and Vila, f. 2009. The damsel bug Nabis pseudoferus (Hem.: Nabidae) as a new biological control agent of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), in tomato crops of Spain. IOBC/WPRS Bull. 49:219–223.
Contreras, J., Mendoza, J. E., Martinez-Aguirre, M. R., Garcia-Vidal, L., Izquierdo, J. and Bielza, P. 2014. Efficacy of Enthomopathogenic Fungus Metarhizium anisopliae Against Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Economic Entomology 107, 121-124.
Cuthbertson, A. G. S, Mathers, J. J., Blackburn, L. F., Korycinska, A., Luo, W., Jacobson, R. J. and Northing, P. 2013. Population development of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under simulated UK glasshouse conditions. Insects. 4: 185–197.
Desneux, N., Wajnberg, E., Wyckhuys, K. A. G., Burgio, G., Arpai, S., Narvaez-Vasquez, C., Gonzalez-Cabrera, A. J., Ruescas, D. C., Tabone, E., Frandon, J., Pizzol, J., Poncet, C., Cabello, T. and Urbaneja, A. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science. 83: 197–215.
Dick, J. T. A., Gallagher, K., Avlijas, S., Clarke, H. C., Lewis, S. E., Leung, S., Minchin, D., Caffrey, J., Alexander, M. E., Maguire, C., Harrod, C., Reid, N., Haddaway, N. R., Farnsworth, K. D., Penk, M. and Ricciardi, A. 2013. Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biological Invasions. 15: 837–846.
Fathipour, Y. and Jafari, A. A. F. 2003. Functional response of preda‌tors Nabis capsiformis and Chrysoperla carnea to different den‌sities of Creontiades pallidus nymphs. Journal of Agriculture Science and Natural Resource. 10: 125–133.
Fernandez-Maldonado, F. J., Gallego, J. R., Valencia, A., Gamez, M., Varga, Z., Garay, J. and Cabello, T. 2017. Cannibalism: Do risks of fighting and reprisal reduce predatory rates? Community Ecology. 18: 87-96.
Gámez, M., Sebestyén, Z., Varga, Z., Garay, J., Gallego, J. R., Fernández, F. J., Cabello, T. 2012. Multi-stage dynamic model for prey-predator interaction: Application to Spodoptera exigua (Lep.: Noctuidae) and Nabis pseudoferus (Hem.: Nabidae) under greenhouse conditions. Integrated Control in Protected Crops, Mediterranean Climate, IOBC-WPRS Bulletin, Vol. 80, p. 184.
Ghaderi, S., Fathipour, Y., Asgari, Sh. 2017. Susceptibility of Seven Selected Tomato Cultivars to Tuta absoluta (Lepidoptera: Gelechiidae): Implications for Its Management. Journal of Economic Entomology. 110: 421-429.
Gharekhani, G. H., Salek-Ebrahimi, H. 2014. Life Table Parameters of Tuta absoluta (Lepidoptera: Gelechiidae) on Different Varieties of Tomato. Journal of Economic Entomology. 107: 1765-1770.
Ghoneim, K. 2014. Predatory insects and arachnids as potential biological control agents against the invasive tomato leaf miner, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. Journal of Entomology and Zoology Studies. 2: 52-71.
Havaskary, M., Farshbaf Pour‌-‌Abad, R., Kazemi, M. H., Rafeii, A. and Havaskary, Sh. 2012. An Investigation to the Fauna of Cimicomorpha (Heteroptera) From Parsabad‌-‌E‌-Moghan and Vicinity, NW Iran. Munis Entomology and Zoology Journal. 7:1101-1107.
Holling, C. S. 1959. Some characteristics of simple types of predation and parasitism. The Canadian Entomologist. 91: 385-399.
Inanl, C. and Oldargc, A. K. 2012. Effects of entomopathogenic fungi, Beauveria bassiana (Bals.) and Metarhizium anisopliae (Metsch.) on larvae and egg stages of Tuta absoluta (Meyrick) Lepidoptera: Gelechiidae. Ege Üniversitesi Ziraat Fakültesi Dergisi. 49: 239-242.
Ingegno, B. L., Ferracini, C., Gallinotti, D., Alma, A. and Tavella, L. 2013. Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biological Control. 67: 246–252.
Inglis, G. D., Enkerli, J. and Goettel, M. S. 2012. Laboratory techniques used for entomopathogenic fungi: Hypocreales. In L. A. Lacey (Ed.), Manual of Techniques in Invertebrate Pathology. (pp. 189-253). Academic Press, London.
Jarrahi, A. and Safavi, S. A. 2016a. Effects of pupal treatment with Proteus® and Metarhizium anisopliae sensu lato on functional response of Habrobracon hebetor parasitizing Helicoverpa armigera in an enclosed experiment system. Biocontrol Science and Technology. 26: 206-216.
Jarrahi, A. and Safavi, S. A. 2016b. Temperature-dependent functional response and host preference of Habrobracon hebetor between fungus-infected and uninfected Ephestia kuehniella larvae. Journal of Stored Products Research. 67: 41-48.
Juliano, S. A. 2001. Non-linear curve fitting: predation and functional response curves. In: Cheiner, S. M., Gurven, J. (Eds.), Design and Analysis of Ecological Experiments. Oxford University Press, New York, pp. 178-196.
Labbe´, R. M., Cloutier, C. and Brodeur, J. 2006. Prey Selection by Dicyphus hesperus of Infected or Parasitized Greenhouse Whitefly. Biocontrol Science and Technology. 16: 485-494.
Labbe´, R. M., Gillespie, D. R., Cloutier, C. and Brodeur, J. 2009. Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Science and Technology. 19: 429-446.
Lester, P. J., Pree, D. J., Thistlewood, H. M. A., Trevisan, L. M. and Harmsen, R. 1999. Pyrethroid encapsulation for the conservation of acarine predators and reduced spider mite (Acari: Tetranychidae) outbreaks in apple orchards. Environmental Entomology. 28: 72–80.
Luna, M. G., Sa´nchez, N. E., Pereyra, P. C., Nieves, E., Savino, V., Luft, E., Virla, E. and Speranza, S. 2012. Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies. Bulletin OEPP/EPPO. 42: 260–267.
Ma, J., Li, Y. Z., Keller, M. and Ren, S. X. 2005. Functional response and predation of Nabis kinbergii (Hemiptera: Nabidae) to Plutella xylostella (Lepidoptera: Plutellidae). Insect Science. 12: 281-286.
Madurappulige, D. 2005. Effect of Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) on Diadegma Semiclausum (Hellen) (Hymenoptera: Ichneumonidae), a Parasitoid of Plutella Xylostella (L.) (Lepidoptera: Yponomeutidae). Lincoln University, New Zealand. PhD Thesis.
Mahdavi, T. S., and Madadi, H. 2015. Biology and life table parameters of Nabis pseudoferus by feeding on cotton aphid Aphis gossypii. Journal of Biological Control of Pests and Plant Diseases. 4: 121-129. (In Farsi with English abstract).
Mahdavi, T. S., and Madadi, H. 2017. Prey preference of Nabis pseudoferus Remane on Aphis gossypii Glover and Tuta absoluta Meyrick. Plant Protection (Scientific Journal of Agriculture). 40: 33-47.
Miranda, M. M. M., Picanco, M., Zanuncio, J. C. and Guedes, R. N. C. 1998. Ecological life table of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Biocontrol Science and Technology. 8: 597-606.
Modarres Awal, M. 2008. Contribution to Heteroptera fauna of Khorasan Razavi province of Iran. Turkish Journal of Entomology. 32: 243-253.
Nozad-Bonab, Z., Hejazi, M. J., Iranipour, S. h. and Arzanlou, M. 2017. Lethal and Sublethal Effects of Some Chemical and Biological Insecticides on Tuta absoluta (Lepidoptera: Gelechiidae) Eggs and Neonates. Journal of Economic Entomology. 110: 1138-1144.
Pires, L., Marques, E., Wanderley-Teixeira, V., Teixeira, Á., Alves, L. and Alves, E. 2008. Ultrastructure of Tuta absoluta parasitized eggs and the reproductive potential of females after parasitism by Metarhizium anisopliae. Micron. 40: 255-261.
Pourian, H. R., Talaei-Hassanloui, R., Kosari, A. A. and Ashouri, A. 2011. Effect of Metarhizium anisopliae on searching, feeding and predation by Orius albidipennis (Hem., Anthocoridae) on Thrips tabaci (Thy., Thripidae). Biocontrol Science and Technology. 21: 15-21.
Propp, G. D. 1982. Functional response of Nabis americoferus to two of its prey, Spodoptera exigua and Lygus hesperus. Environmental Entomology. 11: 670-674.
Rännbäck, L. M., Cotes, B., Anderson, P., Räamert, B. and Meyling, N. Y. 2015. Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae. Journal of Invertebrate Pathology. 124: 78-86.
Rogers, D. 1972. Random search and insect population models. Journal of Animal Ecology. 41: 369–383.
Roy, H. R., Pell, J. K. and Alderson, P. G. 1999. Effects of Fungal Infection on the Alarm Response of Pea Aphids. Journal of Invertebrate Pathology. 74: 69-75.
Roy, H. E. and Pell, J. K. 2000. Interactions Between Entomopathogenic Fungi and Other Natural Enemies: Implications for Biological Control. Biocontrol Science and Technology. 10: 737-752.
Royama, T. 1971. A comparative study of models for predation and parasitism. Researches on Population Ecology Supplement. 1: 1–90.
SAS Institute. 2003. A guide to statistical and data analysis, version 9.1. SAS Institute, Cary, USA.
Scorsetti, A. C., Pelizza, S., Fogel, M.N., Vianna, F. and Schneider, M. I. 2017. Interactions between the entomopathogenic fungus Beauveria bassiana and the Neotropical predator Eriopis connexa (Coleoptera: Coccinellidae): Implications in biological control of pest. Journal of Plant Protection Research. 57: 205-211.
Seiedy, M., Saboori, A., Allahyari, H., Talaei-Hassanloui, R. and Tork, M. 2012. Functional Response of Phytoseiulus persimilis (Acari: Phytoseiidae) on Untreated and Beauveria bassiana _ Treated Adults of Tetranychus urticae (Acari: Tetranychidae). Journal of Insect Behavior. 25: 543-553.
Solomon, M. E. 1949. The natural control of animal populations. Journal of Animal Ecology. 18: 1-35.
Tadele, S. and Emana, G. 2017. Entomopathogenic Effect of Beauveria bassiana (Bals.) and Metarrhizium anisopliae (Metschn.) on Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) Larvae Under Laboratory and Glasshouse Conditions in Ethiopia. Journal of Plant Pathology and Microbiology. 8: 411-414.
Urbaneja, A., González-Cabrera, J., Arnó J. and Gabarra, R. 2012. Prospects for biological control of Tuta. absoluta in tomatoes of the Mediterranean basin. Pest Management Science. 68:1215-1222.
van den Meiracker, R. A. F. and Sabelis, M. W. 1999. Do functional responses of predatory arthropods reach a plateau? A case study of Orius insidiosus with western flower thrips as prey. Entomologia Experimentalis et Applicata. 90: 323–329.
Wekesa, V. W., Moraes, G. J., Knapp, M. and Delalibera- Jr, I. 2007. Interactions of two natural enemies of Tetranychus evansi, the fungal pathogen Neozygites floridana (Zygomycetes: Entomophthorales) and the predatory mite, Phytoseiulus longipes (Acari: Phytoseiidae). Biological Control. 41: 408-414.
Wu, S. Y., Gao, Y. L., Xu, X. N., Goettel, M. S. and Lei, Z. R. 2015. Compatibility of Beauveria bassiana with Neoseiulus barkeri for control of Frankliniella occidentalis. Journal of Integrative Agriculture. 14: 98–105.
Wu, S. Y., Gao, Y. L, Smagghe, G., Xu, X. N. and Lei, Z. R. 2016. Interactions between the entomopathogenic fungus Beauveria bassiana and the predatory mite Neoseiulus barkeri and biological control of their shared prey/host Frankliniella occidentalis. Biological Control. 98: 43–51.
Zappala, L., Biondi, A., Alma, A., Al-Jboory, I. J., Arno, J., Bayram, A., Chailleux, A., El-Arnaouty, A., Gerling, D., Guenaoui, Y., Shaltiel-Harpaz, L., Siscaro, G., Stavrinides, M., Tavella, L., Aznar, R. V., Urbaneja, A. and Desneux, N. 2013. Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. Journal of Pest Science. 86: 635-647.