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Taxonomic identification of Macrolophus pygmaeus and Macrolophus melanotoma based on morphometry and molecular markers

Published online by Cambridge University Press:  24 September 2012

C. Castañé*
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
N. Agustí
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
J. Arnó
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
R. Gabarra
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
J. Riudavets
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
J. Comas
Affiliation:
Universitat Politècnica de Catalunya, Departament d'Enginyeria Agroalimentària i Biotecnologia, C/Esteve Terrades 8, 08860-Castelldefels, Spain
Ó. Alomar
Affiliation:
IRTA, Entomology, Carretera de Cabrils Km 2, 08348-Cabrils, Spain
*
*Author for correspondence Fax: +0034937533954 E-mail: [email protected]

Abstract

Two Macrolophus species, M. melanotoma (=M. caliginosus) and M. pygmaeus, have been referred to as efficient predators of several key pests on vegetable crops in Europe. However, due to the great morphological similarity of these species, they have been confused, with important consequences for inoculative releases of these predators in greenhouses and for the conservation of their natural populations on greenhouse and outdoor crops. In this work, we developed tools to identify these morphologically very similar species. We first confirmed the specific status of two Macrolophus populations collected on their respective host plants (Dittrichia viscosa and tomato) through crossing experiments. Then, using multivariate morphometric analysis, we proposed a linear discriminant function that combines head measurements separating males from the two species without error. Finally, we designed specific primers for a mitochondrial DNA region that were able to distinguish field-collected Macrolophus individuals through conventional PCR. In conclusion, the tools developed in the present study will allow reliable identification of the Macrolophus species present in crops and in the native flora that are the source of populations that colonise them. They will also allow correct identification of mass reared Macrolophus to be introduced in greenhouse crops in inoculative releases.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

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References

Agustí, N. & Gabarra, R. (2009a) Effect of adults age and insect density of Dicyphus tamaninii Wagner (Heteroptera: Miridae) on progeny. Journal of Pest Science 82, 241246.Google Scholar
Agustí, N. & Gabarra, R. (2009b) Puesta a punto de una cría masiva del depredador polífago Dicyphus tamaninii Wagner (Heteroptera: Miridae). Boletín de Sanidad Vegetal: Plagas 35, 205218.Google Scholar
Agustí, N., Unruh, T.R. & Welter, S.C. (2003) Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts by using COI mitochondrial markers. Bulletin of Entomological Research 93, 179185.Google Scholar
Alomar, O., Goula, M. & Albajes, R. (1994) Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonization of tomato fields. IOBC/WPRS Bulletin 17(5), 217223.Google Scholar
Alomar, O., Goula, M. & Albajes, R. (2002) Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agriculture, Ecosystems and Environment 89, 105115.Google Scholar
Alomar, O., Riudavets, J. & Castañé, C. (2006) Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biological Control 36, 154162.Google Scholar
Bagnères, A.G. & Wicker-Thomas, C. (2010) Chemical taxonomy with hydrocarbons. pp. 121162in Blomquist, G.J. & Bagnères, A.G. (Eds) Insect Hydrocarbons. Biology, Biochemistry and Chemical Ecology. Cambridge, UK, Cambridge University Press.Google Scholar
Carapezza, A. (1995) The specific identities of Macrolophus melanotoma (A. Costa, 1853) and Stenodema curticolle (A. Costa, 1853) (Insecta Heteroptera, Miridae). Naturalista Siciliano 19, 295298.Google Scholar
Castañé, C. & Zapata, R. (2005) Rearing the predatory bug Macrolophus caliginosus on a meat-based diet. Biological Control 34, 6672.CrossRefGoogle Scholar
Castañé, C., Alomar, O., Goula, M. & Gabarra, R. (2004) Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biological Control 30, 591597.Google Scholar
Castañé, C., Quero, R. & Riudavets, J. (2006) The brine shrimp Artemia sp. as alternative prey for rearing the predatory bug Macrolophus caliginosus. Biological Control 38, 405412.Google Scholar
Castañé, C., Alomar, O., Riudavets, J. & Gemeno, C. (2007) Reproductive biology of the predator Macrolophus caliginosus: effect of age on sexual maturation and mating. Biological Control 43, 278286.Google Scholar
Cobben, R.H. (1968) Evolutionary Trends in Heteroptera, Part I, Eggs, Architecture of the Shell, Gross Embryology and Eclosion. Wageningen, The Netherlands, Centre for Agricultural Publishing and Documentation.Google Scholar
Constant, B., Grenier, S. & Bonnot, G. (1994) Analysis of some morphological and biochemical characteristics of the egg of the predaceous bug Macrolophus caliginosus (Het.: Miridae) during embryogenesis. BioControl 39, 189198.Google Scholar
Costanzi, M. & Pini, S. (1991) Ruolo di due Miridi predatory nella difesa delle colture ortofloricole. Colture Protette 11, 4953.Google Scholar
Franco, K., Jauset, A. & Castañé, C. (2011) Monogamy and polygamy in two species of mirid bugs: a functional-based approach. Journal of Insect Physiology 57, 307315.CrossRefGoogle ScholarPubMed
Fréchette, B., Rojo, S., Alomar, O. & Lucas, E. (2007) Intraguild predation between syrphids and mirids: who is the prey? Who is the predator? BioControl 52, 175191.Google Scholar
Gabarra, R., Alomar, O., Castañé, C., Goula, M. & Albajes, R. (2004) Movement of the greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses. Agriculture, Ecosystems and Environment 102, 341348.Google Scholar
Gemeno, C., Alomar, O., Riudavets, J. & Castañé, C. (2007) Mating periodicity and post-mating refractory period in the zoophytophagous plant bug Macrolophus caliginosus (Heteroptera: Miridae). European Journal of Entomology 104, 715720.Google Scholar
Gemeno, C., Laserna, N., Riba, M., Valls, J., Castañé, C. & Alomar, O. (2012) Cuticular hidrocarbons discrimínate cryptic Macrolophus species (Hemiptera:Miridae). Bulletin of Entomological Research, doi: 10.1017/S0007485312000193.Google Scholar
Goula, M. & Alomar, O. (1994) Miridos (Heteroptera Miridae) de interés en el control integrado de plagas en tomate. Guía para su identificación. Boletín de Sanidad Vegetal: Plagas 20, 131143.Google Scholar
Hillert, O., Jackel, B. & Plate, H.-P. (2002) Macrolophus pygmaeus (Rambur 1839) (Heteroptera, Miridae)-ein interessanter Nutzling im biologischen Pflanzenschutz. (Macrolophus pygmaeus (Rambur 1839) (Heteroptera, Miridae)-an important benificial organism for biological methods). Gesunde Pflanzen 54, 6673.Google Scholar
Ingegno, B.L., Pansa, M.G. & Tavella, L. (2009) Tomato colonization by predatory bugs (Heteroptera: Miridae) in agroecosystems of NW Italy. IOBC/WPRS Bulletin 49, 287291.Google Scholar
Josifov, M. (1992) Zur Taxonomie der paläarktischen Macrolophus-Arten (Insecta, Heteroptera: Miridae). Reichenbachia 29, 14.Google Scholar
Kerzhner, I.M. & Josifov, M. (1999) Cimicomorpha II: Miridae. pp. 2527in Aukema, B. & Rieger, C. (Eds) Catalogue of the Heteroptera of the Palaearctic Region. Wageningen, The Netherlands, Netherlands Entomological Society.Google Scholar
Lucas, E. & Alomar, O. (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biological Control 20, 147152.Google Scholar
Lucas, E. & Alomar, O. (2002a) 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
Lucas, E. & Alomar, O. (2002b) Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits. Journal of Economic Entomology 95, 11231129.Google Scholar
Lucas, E., Fréchette, B. & Alomar, O. (2009) Resource quality, resource availability, and intraguild predation among omnivorous mirids. Biocontrol, Science and Technology 19, 555572.Google Scholar
Lundgren, J.G. (2011) Reproductive ecology of predaceous Heteroptera. Biological Control 59, 3752.Google Scholar
Lykouressis, D., Perdikis, D. & Chalkia, Ch. (2000a) The effects of natural enemies on aphid populations on processing tomato. Entomologia Hellenica [1999–2000] 13, 3542.Google Scholar
Lykouressis, D., Perdikis, D. & Tsagarakis, A. (2000b) Polyphagous mirids in Greece: Host plants and abundance in traps placed in some crops. Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri 56, 5768.Google Scholar
Machtelinckx, T., Van Leeuwen, T., Vanholme, B., Gehesquière, B., Dermauw, W., Vandekerkhove, B., Gheysen, G. & De Clercq, P. (2009) Wolbachia induces strong cytoplasmic incompatibility in the predatory bug Macrolophus pygmaeus. Insect Molecular Biology 18, 373381.Google Scholar
Malausa, J.C. (1989) Lutte integrée sous serre: Les punaises prédatrices Mirides dans les cultures de solanacées du sud-est de la France. Revue Horticole 298, 3943.Google Scholar
Malausa, J.C. & Trottin-Caudal, Y. (1996) Advances in the strategy of use of the predaceous bug Macrolophus caliginosus (Heteroptera: Miridae) in glasshouse crops. pp. 178189in Alomar, O. & Wiedenmann, R.N. (Eds) Zoophytophagous Heteroptera: Implications for Life History and Integrated Pest Management. Lanham, MD, USA, Entomological Society of America.Google Scholar
Martinez-Cascales, J.I., Cenis, J.L., Cassis, G. & Sánchez, J.A. (2006) Species identity of Macrolophus melanotoma (Costa 1853) and Macrolophus pygmaeus (Rambur 1839) (Insecta: Heteroptera: Miridae) based on morphological and molecular data and bionomic implications. Insect Systematics and Evolution 37, 385404.Google Scholar
Montserrat, M., Albajes, R. & Castañé, C. (2004) Behavioral responses of three plant-inhabiting predators to different prey densities. Biological Control 30, 256264.Google Scholar
Moreno-Ripoll, R. (2011) Control biológico de moscas blancas en cultivo de tomate: interacciones entre sus enemigos naturales. PhD thesis, University of Barcelona. Barcelona, Spain.Google Scholar
Perdikis, D. & Lykouressis, D. (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biological Control 17, 5560.Google Scholar
Perdikis, D. & Lykouressis, D. (2002) Description of the eggs and the nymphal instars of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Entomologia Hellenica 14, 3240.Google Scholar
Perdikis, D.C., Margaritopoulos, J.T., Stamatis, C., Mamuris, Z., Lykouressis, D.P., Tsitsipis, J.A. & Pekas, A. (2003) Discrimination of the closely related biocontrol agents Macrolophus melanotoma (Hemiptera: Miridae) and M. pygmaeus using mitochondrial DNA analysis. Bulletin of Entomological Research 93, 507514.Google Scholar
Perdikis, D., Favasa, C., Lykouressis, D. & Fantinou, A. (2007) Ecological relationships between non-cultivated plants and insect predators in agroecosystems: the case of Dittrichia viscosa (Asteraceae) and Macrolophus melanotoma (Hemiptera: Miridae). Acta Oecologica 31, 299306.Google Scholar
Perdikis, D., Fantinou, A. & Lykouressis, D. (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biological Control 59, 1321.CrossRefGoogle Scholar
Pérez, T., Albornoz, J. & Domínguez, A. (1998) An evaluation of RAPD fragment reproducibility and nature. Molecular Ecology 7, 13471357.Google Scholar
Rabouam, C., Comes, A.M., Bretagnolle, V., Humbert, J.F., Periquet, G. & Bigot, Y. (1999) Features of DNA fragments obtained by random amplified polymorphic DNA (RAPD) assays. Molecular Ecology 8, 493503.Google Scholar
Rosen, D. & DeBach, P. (1973) Systematics, morphology and biological control. Entomophaga 18, 215222.Google Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org (accessed 4 August 2012).Google Scholar
Schlick-Steiner, B.C., Steiner, F.M., Seifert, B., Stauffer, C., Christian, E. & Crozier, R.H. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55, 421–38.Google Scholar
Schmidt, J.E.U., Almeida, J.R.M., Rosati, C. & Arpaia, S. (2009) Identification of trophic interactions between Macrolophus caliginosus (Heteroptera: Miridae) and Myzus persicae (Homoptera: Aphididae) using real time PCR. BioControl 54, 383391.Google Scholar
Stichel, W. (1962) Illustrierte Bestimmungstabellen der Wanzen. II Europa (Hemiptera-Heteroptera Europae), vols 1–4. Berlin-Hermsdorf, Germany.Google Scholar
Tavella, L. & Goula, M. (2001) Dicyphini collected in horticultural areas of north-western Italy (Heteroptera Miridae). Bollettino di Zoologia Agraria e di Bachicoltura 33, 93102.Google Scholar
Urbaneja, A., González-Cabrera, J., Arnó, J. & Gabarra, R. (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Management Science 68, 12151222.Google Scholar
van Lenteren, J.C. (2003) Commercial availability of biological control agents. pp. 167179in van Lenteren, J.C. (Ed.) Quality Control and Production of Biological Control Agents, Theory and Testing Procedures. Oxon, UK, CABI Publishing.Google Scholar
Wagner, E. (1951) Contributo alla conoscenza della fauna emitterologica italiana. II. Zwei neue Miriden-Arten und eine bisher übersehene Art aus Italien (Hem. Het.). B. Macrolophus caliginosus n. sp., eine neue Miridenart aus Italien (Hem. Het.). Bollettino dell'Associazione Romana di Entomologia 5, 2931.Google Scholar
Wagner, E. (1974) Die Miridae Hahn, 1831 des Mittelmeerraumes und der Makaronesischen Inseln (Hemiptera, Heteroptera), Teil 1. Entomologische Abhandlungen, herausgegeben vom Staatlichen Museum für Naturkunde Dresden 37, Suppl. (1970–1971), i–ii, 1484.Google Scholar