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Biological traits of the predatory mirid Macrolophus praeclarus, a candidate biocontrol agent for the Neotropical region

Published online by Cambridge University Press:  15 February 2021

Meritxell Pérez-Hedo*
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología. Unidad de Entomología. Carretera CV-315, Km 10'7 - 46113Moncada, Spain
Carolina Gallego
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología. Unidad de Entomología. Carretera CV-315, Km 10'7 - 46113Moncada, Spain
Amy Roda
Affiliation:
United States Department of Agriculture, Animal Plant Health Inspection Service, Plant Protection and Quarantine, Science and Technology, Miami, Florida33158, USA
Barry Kostyk
Affiliation:
Department of Entomology and Nematology, University of Florida, Southwest Florida Research and Education Center, Immokalee, Florida34142, USA
Mónica Triana
Affiliation:
Department of Entomology and Nematology, University of Florida, Southwest Florida Research and Education Center, Immokalee, Florida34142, USA
Fernando Alférez
Affiliation:
University of Florida, Department of Horticultural Sciences, Southwest Florida Research and Education Center, Immokalee, Florida34142, United States of America
Philip A. Stansly
Affiliation:
Department of Entomology and Nematology, University of Florida, Southwest Florida Research and Education Center, Immokalee, Florida34142, USA
Jawwad Qureshi
Affiliation:
Department of Entomology and Nematology, University of Florida, Southwest Florida Research and Education Center, Immokalee, Florida34142, USA
Alberto Urbaneja
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología. Unidad de Entomología. Carretera CV-315, Km 10'7 - 46113Moncada, Spain
*
Author for correspondence: Meritxell Pérez-Hedo, Email: mperezh@ivia.es

Abstract

The predatory mirid Macrolophus praeclarus is widely distributed throughout the Americas, and is reported to prey upon several horticultural pest species. However, little is known about its biology, thermal requirements, crop odour preferences, phytophagy, and capability to induce defensive responses in plants. When five temperatures studied (20, 25, 30, 33 and 35°C) were tested and Ephestia kuehniella was used as prey, the developmental time from egg to adult on tomato, was longest at 20°C (56.3 d) and shortest at 33°C (22.7 d). The ability of nymphs to develop to adults decreased as the temperature increased, with the highest number of nymphs reaching the adult stage at 20°C (78.0%) and lowest at 35°C (0%). The lower and upper developmental thresholds were estimated at 11.2° and 35.3°C, respectively. The maximum developmental rate occurred at 31.7°C and the thermal constant was 454.0 ± 8.1 degree days. The highest predation rate of E. kuehniella eggs was obtained at 30°C. In Y-tube olfactory choice tests, M. praeclarus selected tomato, sweet pepper and eggplant odours more frequently than no plant control treatment. Macrolophus praeclarus feeding did not damage tomato plants compared to another zoophytophagous mirid, Nesidiocoris tenuis, which caused necrotic rings. The phytophagy of M. praeclarus induced defensive responses in tomato plants through the upregulation of the jasmonic acid metabolic pathway. The implications of the findings for using M. praeclarus in tomato biological control programmes in the Americas are discussed.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

Deceased

References

Abbas, S, Pérez-Hedo, M, Colazza, S and Urbaneja, A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl 59, 565574.CrossRefGoogle Scholar
Arellano, G and Vergara, C (2016) Especies de Miridae (Hemiptera) registradas en algunos cultivos tropicales en Chanchamayo y Satipo (Junín, Perú). Ecología Aplicada 15, 101106.CrossRefGoogle Scholar
Arnó, J, Gabarra, R, Liu, TX, Simmons, AM and Gerling, D (2010) Natural enemies of Bemisia tabaci: predators and parasitoids. In Stansly, PA and Naranjo, SE (eds), Bemisia: Bionomics and Management of a Global Pest. Dordrecht-Heidelberg-London-New York: Springer, pp. 385421.Google Scholar
Ayala, JL, Grillo, H and Vera, ER (1982) Enemigos naturales de Heliothis virescens (Fabricius) (Lepidoptera: Noctuidae) en las provincias centrales de Cuba. Centro Agrícola 9, 314.Google Scholar
Biondi, A and Desneux, N (2019) Special issue on Tuta Absoluta: recent advances in management methods against the background of an ongoing worldwide invasion. Journal of Pest Science 92, 13131315.CrossRefGoogle Scholar
Bouagga, S, Urbaneja, A, Rambla, JL, Flors, V, Granell, A, Jaques, JA and Pérez-Hedo, M (2018) Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants. Pest Management Science 74, 12861296.CrossRefGoogle ScholarPubMed
Bouagga, S, Urbaneja, A, Depalo, L, Rubio, L and Pérez-Hedo, M (2020) Zoophytophagous predator-induced defences restrict accumulation of the tomato spotted wilt virus. Pest Management Science 76, 561567.CrossRefGoogle ScholarPubMed
Bouvet, JPR, Urbaneja, A, Pérez-Hedo, M and Monzó, C (2019) Contribution of predation to the biological control of a key herbivorous pest in citrus agroecosystems. Journal of Animal Ecology 88, 915926.CrossRefGoogle ScholarPubMed
Bueno, VHP, van Lenteren, JC, Lins, JC, Calixto, AM, Montes, FC, Silva, DB, … Pérez, LM (2013) New records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) predation by Brazilian Hemipteran predatory bugs. Journal of Applied Entomology 137, 2934.CrossRefGoogle Scholar
Bueno, VHP, Montes, FC, Sampaio, MV, Calixto, AM and van Lenteren, JC (2018) Performance of immatures of three neotropical miridae at five different temperatures, reared on Ephestia kuehniella eggs on tobacco plants. Bulletin of Insectology 71, 7787.Google Scholar
Calvo, FJ, Torres-Ruiz, A, Velázquez-González, JC, Rodríguez-Leyva, E and Lomeli-Flores, JR (2016) Evaluation of Dicyphus hesperus for biological control of sweet potato whitefly and potato psyllid on greenhouse tomato. BioControl 61, 415424.CrossRefGoogle Scholar
Campbell, A, Frazer, B, Gilbert, N, Gutierrez, AP and Mackauer, M (1974) Temperature requirements of somea aphids and their parasites. Journal of Applied Ecology 11, 431438.CrossRefGoogle Scholar
Carvalho, JCM and Rosas, AF (1965) Mirídeos neotropicais, XCV: Gênero e espécies nova do Suriname, com uma lista de espécies coligidas em Paramarimbo (Hemiptera). Revista Brasileira de Biologia 25, 207210.Google Scholar
Carvalho, JOSCM, Da, R, Afonso, S, Paulo, D and Roberto, P (1977) Mirídeos neotropicais, CCVIII: Sobre uma colecao enviada para estudo pela academia de ciencias da california (Hemiptera). Revista Brasileira de Biologia 37, 716.Google Scholar
Cassis, G (1984) A Systematic Study of the Subfamily Dicyphinae (Heteroptera: Miridae) (PhD Thesis). Oregon State University. Retrieved from https://ir.library.oregonstate.edu/concern/graduate_thesis_or_dissertations/1g05ff581.Google Scholar
Chérot, F and Carpintero, DL (2016) New and little-known miridae from French Guyana and neighbouring areas (Hemiptera: Heteroptera). Entomologica Americana 122, 8296.CrossRefGoogle Scholar
Chérot, F, Carpintero, DL and Maes, JM (2007) Sur une collection de Miridae du Nicaragua (Insecta, Heteroptera). Nouvelle Revue d'Entomologie 23, 173190.Google Scholar
Chinchilla-Ramírez, M, Pérez-Hedo, M, Pannebakker, BA and Urbaneja, A (2020) Genetic variation in the feeding behavior of isofemale lines of Nesidiocoris tenuis. Insects 11, 513.CrossRefGoogle ScholarPubMed
Chinchilla-Ramírez, M, Garzo, E, Fereres, A, Gavara-Vidal, J, ten Broeke, CJ, van Loon, JJA, … Pérez-Hedo, M (2021) Plant feeding by Nesidiocoris tenuis: quantifying its behavioral and mechanical components. Biological Control 152, 104402.CrossRefGoogle Scholar
Ferreira, PSF and Henry, TJ (2011) Synopsis and keys to the tribes, genera, and species of Miridae (Hemiptera: Heteroptera) of minas gerais, Brazil part I: Bryocorinae. Zootaxa 2920, 141.CrossRefGoogle Scholar
Hart, AJ, Tullett, AG, Bale, JS and Walters, KFA (2002) Effects of temperature on the establishment potential in the U.K. of the non-native glasshouse biocontrol agent Macrolophus caliginosus. Physiological Entomology 27, 112123.CrossRefGoogle Scholar
IBM SPSS (2004) SPSS v. 22 for Windows. Chicago, IL: SPSS Inc.Google Scholar
Janzen, DH (1967) Why mountain passes are higher in the tropics. The American Naturalist 101, 233249.CrossRefGoogle Scholar
Lactin, DJ, Holliday, NJ, Johnson, DL and Craigen, R (1995) Improved rate model of temperature-dependent development by arthropods. Environmental Entomology 24, 6875.CrossRefGoogle Scholar
Lellani, H, Díaz, B, Li, EL, Li, NM, Martínez, MDLÁ, Rivero, I, … Bueno, P (2014) Life table of Macrolophus basicornis (Hemiptera: Miridae) preying on Myzus persicae (Sulzer) and Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae). Revista de Protección Vegetal 29, 9498.Google Scholar
Lucas, É and Alomar, O (2002a) Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits. Journal of Economic Entomology 95, 11231129.CrossRefGoogle Scholar
Lucas, É and Alomar, O (2002b) Impact of the presence of Dicyphus tamaninii Wagner (Heteroptera: Miridae) on whitefly (Homoptera: Aleyrodidae) predation by Macrolophus caliginosus (Wagner) (Heteroptera: Miridae). Biological Control 25, 123128.CrossRefGoogle Scholar
Martínez, MA, Duarte, L, Baños, HL, Rivas, A and Sánchez, A (2014) Predatory mirids (Hemiptera: Heteroptera: Miridae) in tomato and tobacco in Cuba. Revista de Protección Vegetal 29, 204207.Google Scholar
Martínez-García, H, Sáenz-Romo, MG, Aragón-Sánchez, M, Román-Fernández, LR, Sáenz-de-Cabezón, E, Marco-Mancebón, VS and Pérez-Moreno, I (2017) Temperature-dependent development of Macrolophus pygmaeus and its applicability to biological control. BioControl 62, 481493.CrossRefGoogle Scholar
Mollá, O, Biondi, A, Alonso-Valiente, M and Urbaneja, A (2014) A comparative life history study of two mirid bugs preying on Tuta Absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl 59, 175183.CrossRefGoogle Scholar
Pappas, ML, Steppuhn, A, Geuss, D, Topalidou, N, Zografou, A, Sabelis, MW and Broufas, GD (2015) Beyond predation: the zoophytophagous predator Macrolophus pygmaeus induces tomato resistance against spider mites. PLoS One 10, e0127251.CrossRefGoogle ScholarPubMed
Perdikis, DC and Lykouressis, DP (2002) Thermal requirements for development of the polyphagous predator Macrolophus pygmaeus (Hemiptera: Miridae). Environmental Entomology 31, 661667.CrossRefGoogle Scholar
Pérez-Hedo, M and Urbaneja, A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. Journal of Pest Science 88, 6573.CrossRefGoogle Scholar
Pérez-Hedo, M and Urbaneja, A (2016) The zoophytophagous predator Nesidiocoris tenuis: a successful but controversial biocontrol agent in tomato crops. In Horowitz, AR and Ishaaya, I (eds), Advances in Insect Control and Resistance Management. Dordrecht-Heidelberg-London-New York: Springer, pp. 121138.CrossRefGoogle Scholar
Pérez-Hedo, M, Bouagga, S, Jaques, JA, Flors, V and Urbaneja, A (2015) Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae). Biological Control 86, 4651.CrossRefGoogle Scholar
Pérez-Hedo, M, Suay, R, Alonso, M, Ruocco, M, Giorgini, M, Poncet, C and Urbaneja, A (2017) Resilience and robustness of IPM in protected horticulture in the face of potential invasive pests. Crop Protection 97, 119127.CrossRefGoogle Scholar
Pérez-Hedo, M, Arias-Sanguino, ÁM and Urbaneja, A (2018) Induced tomato plant resistance against Tetranychus urticae triggered by the phytophagy of Nesidiocoris tenuis. Frontiers in Plant Science 9, 1419.CrossRefGoogle ScholarPubMed
Pérez-Hedo, M, Riahi, C and Urbaneja, A (2021) Use of zoophytophagous mirid bugs in horticultural crops: current challenges and future perspectives. Pest Management Science 77, 3342.CrossRefGoogle ScholarPubMed
Roda, A, Castillo, J, Allen, C, Urbaneja, A, Pérez-Hedo, M, Weihman, S and Stansly, PA (2020) Biological control potential and drawbacks of three zoophytophagous mirid predators against Bemisia tabaci in the United States. Insects 11, 670.CrossRefGoogle ScholarPubMed
Rosner, H (2013) Climate adaptation: survival of the flexible. Nature 494, 2223.CrossRefGoogle ScholarPubMed
RStudio Team (2015) RStudio: Integrated Development for R. Boston, MA: RStudio, Inc.Google Scholar
Serra, C and van Lenteren, JC (2020) Biological control in the Dominican Republic. In van Lenteren, JC, Bueno, VHP, Luna, MG and Colmeneraz, YC (eds), Biological Control in Latin America and the Caribbean: Its Rich History and Bright Future. Walingford, UK: CABI Publishing, pp. 199219.CrossRefGoogle Scholar
Silva, DB, Bueno, VHP, Montes, FC and van Lenteren, JC (2016) Population growth of three mirid predatory bugs feeding on eggs and larvae of Tuta absoluta on tomato. BioControl 61, 545553.CrossRefGoogle Scholar
Shipp, JL and Wang, K (2006) Evaluation of Dicyphus hesperus (Heteroptera: Miridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomato. Journal of Economic Entomology 99, 414420.CrossRefGoogle ScholarPubMed
Smith, HA and Krey, KL (2019) Three release rates of Dicyphus hesperus (Hemiptera: Miridae) for management of Bemisia tabaci (Hemiptera: Aleyrodidae) on greenhouse tomato. Insects 10, 213.CrossRefGoogle ScholarPubMed
Soto, SS and Nakano, O (2009) The occurrence of Macrolophus praeclarus (Distant) Hemiptera: Miridae) in the state of São Paulo, Brazil. Revista de Agricultura Piracicaba 84, 149151.Google Scholar
Stansly, PA and Naranjo, SE (2010) Bemisia: Bionomics and Management of A Global Pest. Dordrecht-Heidelberg-London-New York: Springer.CrossRefGoogle Scholar
Sylla, S, Brévault, T, Diarra, K, Bearez, P and Desneux, N (2016) Life-history traits of Macrolophus pygmaeus with different prey foods. PLoS One 11, e0166610.CrossRefGoogle ScholarPubMed
Symondson, WOC, Sunderland, KD and Greenstone, MH (2002) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561594.CrossRefGoogle ScholarPubMed
Tembrock, LR, Timm, AE, Zink, FA and Gilligan, TM (2019) Phylogeography of the recent expansion of Helicoverpa armigera (Lepidoptera: Noctuidae) in South America and the Caribbean Basin. Annals of the Entomological Society of America 112, 388401.CrossRefGoogle Scholar
Urbaneja, A, Tapia, G and Stansly, P (2005) Influence of host plant and prey availability on developmental time and surviorship of Nesidiocoris tenius (Het.: Miridae). Biocontrol Science and Technology 15, 513518.CrossRefGoogle Scholar
Urbaneja, A, González-Cabrera, J, Arnó, J and Gabarra, R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Management Science 68, 12151222.CrossRefGoogle ScholarPubMed
Urbaneja-Bernat, P, Mollá, O, Alonso, M, Bolkcmans, K, Urbaneja, A and Tena, A (2015) Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato. Journal of Applied Entomology 139, 161167.CrossRefGoogle Scholar
Urbaneja-Bernat, P, Bru, P, González-Cabrera, J, Urbaneja, A and Tena, A (2019) Reduced phytophagy in sugar-provisioned mirids. Journal of Pest Science 92, 11391148.CrossRefGoogle Scholar
van Lenteren, JC, Bolckmans, K, Köhl, J, Ravensberg, WJ and Urbaneja, A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63, 3959.CrossRefGoogle Scholar
van Lenteren, JC, Bueno, VHP, Burgio, G, Lanzoni, A, Montes, FC, Silva, DB, … Hemerik, L (2019) Pest kill rate as aggregate evaluation criterion to rank biological control agents: a case study with Neotropical predators of Tuta absoluta on tomato. Bulletin of Entomological Research 109, 812820.CrossRefGoogle ScholarPubMed
van Lenteren, JC, Alomar, O, Ravensberg, WJ and Urbaneja, A (2020) Integrated pest and disease management in greenhouse crops. In Gullino, ML, Albajes, R and Nicot, PC (eds), Integrated Pest and Disease Management in Greenhouse Crops, Plant Pathology in the 21st Century 9, Dordrecht-Heidelberg-London-New York: Springer, pp. 409439.CrossRefGoogle Scholar
Vera, ER and Ayala, JL (1979) Martynia annua L.: planta hospedera de los principales insectos del tabaco. Centro Agrícola 6, 314.Google Scholar
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