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Host Plant Perception and Selection in the Sibling Species Macrolophus melanotoma and Macrolophus pygmaeus (Hemiptera: Miridae)

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Abstract

The electroantennogram responses (EAGs) of Macrolophus melanotoma and Macrolophus pygmaeus (Hemiptera: Miridae) exposed to volatile compounds (VOCs) of host and non-host plants were compared. The VOCs were identified by gas chromatography. Hosts and non-hosts eliciting similar EAGs were tested in olfactory assays against plants without a significant EAGs for the two Macrolophus species. No characteristic VOC profile was found for hosts and non-hosts. Terpenes predominated in many hosts and carboxylic acids in non-hosts, but no specific VOCs were characteristic of host plants. Significant EAGs (maximum deflection values in mV) were recorded in plants with very different VOC profiles, both hosts and non-hosts. The EAGs were higher for M. melanotoma than for M. pygmaeus, and were higher for males than for females. In M. melanotoma the EAGs were greater with hosts than with non-hosts, but they were similar in M. pygmaeus. The EAGs were correlated with the concentrations of sesquiterpenes and alcohols in both species. In olfactory assays, M. melanotoma and M. pygmaeus preferred their respective hosts, but they did not discriminate between non-host with and without significant EAGs. According to the results, Macrolophus species are expected to rely on ubiquitous VOCs for the identification of their hosts. The variation in the EAGs between M. melanotoma and M. pygmaeus is attributed to the variation in the proportions of olfactory receptor neurones with different sensitivity to VOCs (e.g. sesquiterpenes). Host plant selection is discussed in the light of the perception of VOCs and the processing of information by the central nervous system.

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References

  • Alomar Ó, Albajes R (1996) Greenhouse whitefly (Homoptera: Aleyrodidae) predation and tomato fruit injury by the zoophytophagous predator Dicyphus tamaninii (Heteroptera-Miridae). In: Alomar Ó, Wiedenmann RN (eds) Zoophytophagous Heteroptera: implications for life history and Integrated Pest Management. Entomological Society of America, Lanham, pp 155–177

    Google Scholar 

  • Alomar Ó, Castañe C, Gabarra R, Albajes R (1994) Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonization of tomato fields. IOBC WPRS Bull 17:217–223

    Google Scholar 

  • Alomar Ó, Gabarra R, González O, Arnó J (2006) Selection of insectary plants for ecological infrastructure in Mediterranean vegetable crops. IOBC WPRS Bull 29:5–8

    Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman & Hall, New York

    Book  Google Scholar 

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects - finding the right mix. Phytochemistry 72:1605–1611

    Article  CAS  PubMed  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  PubMed  Google Scholar 

  • Calvo J, Blockmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. Biocontrol 54:237–246

    Article  Google Scholar 

  • Cassis G (1986) A systematic study of the subfamily Dicyphinae (Heteroptera, Miridae), Ph.D. Thesis, Oregon State University, University Microfilms International, Ann Arbor, USA

  • Cassis G, Schuh RT (2012) Systematics, biodiversity, biogeography, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annu Rev Entomol 57:377–404

    Article  CAS  PubMed  Google Scholar 

  • Castañe C, Agustí J, Gabarra R, Riudavets J, Comas J, Alomar Ó (2013) Taxonomic identification of Macrolophus melanotoma based on morphometry and molecular markers. Bull Entomol Res 103:204–215

    Article  PubMed  Google Scholar 

  • Chen H, Zhao Y, Kang L (2004) Comparison of the olfactory sensitivity of two sympatric steppe grasshopper species (Orthoptera: Acrididae) to plant volatile compounds. Sci China Ser C Life Sci 47(2):115–123

    Article  CAS  Google Scholar 

  • Christensen T, Hildebrand JG (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12:393–399

    Article  CAS  PubMed  Google Scholar 

  • Couladis M, Chinou IB, Tzakou O, Loukis A (2002) Composition and antimicrobial activity of the essential oil of Ballota pseudodictamnus (L.) Bentham. Phytother Res 16:723–726

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Development Core Team R (2008) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dicke M (1994) Local and systemic production of volatile herbivore-induced terpenoids - their role in plant-carnivore mutualism. J Plant Physiol 143:465–472

    Article  CAS  Google Scholar 

  • Dicke M (2000) Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective. Biochem Syst Ecol 28:601–617

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249

    Article  CAS  Google Scholar 

  • Farhat MB, Jordan MJ, Chaouech-Hamada R, Landoulsi A, Sotomayor JA (2009) Variations in essential oil, phenolic compounds, and antioxidant activity of Tunisian cultivated Salvia officinalis L. J Agr Food Chem 57:10349–10356

    Article  Google Scholar 

  • Fraser AM, Mechaber WL, Hildebrand JG (2003) Electroantennographic and behavioral responses of the sphinx moth Manduca sexta to host plant headspace volatiles. J Chem Ecol 29(8):1813–1833

    Article  CAS  PubMed  Google Scholar 

  • Frati F, Salerno G, Conti E, Bin F (2008) Role of the plant-conspecific complex in host location and intra-specific communication of Lygus rugulipennis. Physiol Entomol 33:129–137

    Article  Google Scholar 

  • Fuyama Y (1978) Behavior genetics of olfactory responses in Drosophila. II. Odorant-specific variant in a natural-population of Drosophila melanogaster. Behav Genet 8:399–414

    Article  CAS  PubMed  Google Scholar 

  • Gazim ZC, Ferreira GA, Rezende CM, Nakamura CV, Dias Filho BP, Cortez DAG (2007) Identificação dos constituintes químicos da fração volátil da Calendula officinalis produzida no Paraná. Hortic Bras 25:118–121

    Article  Google Scholar 

  • Ginzel MD, Hanks LM (2005) Role of host plant volatiles in mate location for three species of longhorned beetles. J Chem Ecol 31:213–217

    Article  CAS  PubMed  Google Scholar 

  • Goula M (1989) Catàleg dels Miridae (Heteroptera) del massís del Garraf. Sessió Conjunta d’Entomologia ICHN-SCL 5:67–76

  • Goula M, Alomar Ó (1994) Miridos (Heteroptera: Miridae) de interés en el control integrado de plagas en tomate. Guía para su identificación. Boletín de Sanidad Vegetal, Plagas 20:131–143

  • Groot AT, Timmer R, Gort G, Lelyveld GP, Drijfhout FP, Van Beek TA, Visser JH (1999) Sex-related perception of insect and plant volatiles in Lygocoris pabulinus. J Chem Ecol 25:2357–2371

    Article  CAS  Google Scholar 

  • Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:718–732

    Article  CAS  Google Scholar 

  • Hardie J, Visser JH, Piron PGM (1995) Peripheral odour perception by adult aphid forms with the same genotype but different host-plant preferences. J Insect Physiol 41:91–97

    Article  CAS  Google Scholar 

  • Ingegno BL (2011) Distribution and bioethology of generalist Dicyphine predators (Hemiptera: Miridae), Ph.D. Thesis, University of Torino, Italy

  • Ingegno BL, Goula M, Navone P, Tavella L (2008) Distribution and host plants of the genus Dicyphus in the Alpine valleys of NW Italy. Bull Insectol 61:139–140

    Google Scholar 

  • Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181

    Article  Google Scholar 

  • Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252

    Article  Google Scholar 

  • Lacey ES, Ginzel MD, Millar JG, Hanks LM (2004) Male-produced aggregation pheromone of the cerambycid beetle Neoclytus acuminatus acuminatus. J Chem Ecol 30:1493–1507

    Article  CAS  PubMed  Google Scholar 

  • Lins JJC, van Loon JJ, Bueno VH, Lucas-Barbosa D, Dicke M, van Lenteren JC (2014) Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics. BioControl 59:707–718

    Article  Google Scholar 

  • Luning PA, De Rijk T, Wichers HJ, Roozen JP (1994) Gas chromatography, mass spectrometry, and sniffing port analyses of volatile compounds of fresh bell peppers (Capsicum annuum) at different ripening stages. J Agric Food Chem 42(4):977–983

    Article  CAS  Google Scholar 

  • Lykouressis D, Perdikis DC, Tsagarakis A (2000) Polyphagous mirids in Greece: host plants and abundance in traps placed in some crops. Boll Lab Entomol Agrar “Filippo Silvestri” 56:57–68

    Google Scholar 

  • Marongiu B, Piras A, Pani F, Porcedda S, Ballero M (2003) Extraction, separation and isolation of essential oils from natural matrices by supercritical CO2. Flavour Fragr J 18:505–509

    Article  CAS  Google Scholar 

  • Martinez-Cascales JI, Cenis JL, Cassis G, Sanchez JA (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 Syst Evol 37:385–404

    Article  Google Scholar 

  • Moayeri HRS, Ashouri A, Brodsgaard HF, Enkegaard A (2006a) Odour-mediated preference and prey preference of Macrolophus caliginosus between spider mites and green peach aphids. J Appl Entomol 130:504–508

    Article  Google Scholar 

  • Moayeri HRS, Ashouri A, Brodsgaard HF, Enkegaard A (2006b) Odour-mediated responses of a predatory mirid bug and its prey, the two-spotted spider mite. Exp Appl Acarol 40:27–36

    Article  PubMed  Google Scholar 

  • Moayeri HRS, Ashouri A, Brodsgaard HF, Enkegaard A (2007a) Males of the predatory mirid bug Macrolophus caliginosus exploit plant volatiles induced by conspecifics as a sexual synomone. Entomol Exp Appl 123:49–55

    Article  CAS  Google Scholar 

  • Moayeri HRS, Ashouri A, Poll L, Enkegaard A (2007b) Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory (vol 131, pg 326, 2007). J Appl Entomol 131:504

    Article  Google Scholar 

  • Ogundajo AL, Oladosu IA, Ogunwande IA, Flamini G, Owolabi MS (2013) Study on the volatile constituents of Solanum nigrum var. virginicum L. from Nigeria. Asian J Plant Sci Res 3(1):94–98

    CAS  Google Scholar 

  • Paolini J, Tomi P, Bernardini AF, Bradesi P, Casanova J, Kaloustian J (2008) Detailed analysis of the essential oil from Cistus albidus L. by combination of GC/RI, GC/MS and 13C-NMR spectroscopy. Nat Prod Res 22(14):1270–1278

    Article  CAS  PubMed  Google Scholar 

  • Park KC, Hardie J (1998) An improved aphid electroantennogram. J Insect Physiol 44:919–928

    Article  CAS  PubMed  Google Scholar 

  • Perdikis DC, Margaritopoulos JT, Stamatis C, Mamuris Z, Lykouressis DP, Tsitsipis JA, Pekas A (2003) Discrimination of the closely related biocontrol agents Macrolophus melanotoma (Hemiptera: Miridae) and M. pygmaeus using mitochondrial DNA analysis. Bull Entomol Res 93:507–514

    CAS  PubMed  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 Oecol 31:299–306

    Article  Google Scholar 

  • Perdikis DC, Kapaxidi E, Papadoulis G (2008) Biological control of insect and mite pests in greenhouse solanaceous crops. Eur J Plant Sci and Biotech 2:125–144

    Google Scholar 

  • Ryan MF (2002) Insect chemoreception. Fundamental and applied. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Sanchez JA (2008) Zoophytophagy in the plantbug Nesidiocoris tenuis. Agric For Entomol 10:75–80

    Article  Google Scholar 

  • Sanchez JA (2009) Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol Control 51:493–498

    Article  Google Scholar 

  • Sanchez JA, Martinez-Cascales JI, Lacasa A (2003) Abundance and wild host plants of predator mirids (Heteroptera: Miridae) in horticultural crops in the Southeast of Spain. IOBC WPRS Bull 26:147–151

    Google Scholar 

  • Sanchez JA, Gillespie DR, McGregor RR (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomol Exp Appl 112:7–19

    Article  Google Scholar 

  • Sanchez JA, Martinez-Cascales JI, Cassis G (2006a) Description of a new species of Dicyphus Fieber (Insecta: Heteroptera: Miridae) from Portugal based on morphological and molecular data. Insect Syst Evol 37:281–300

    Article  Google Scholar 

  • Sanchez JA, Pino-Perez M, del Davó M, Martinez-Cascales JI, Lacasa A (2006b) Zoophytophagy of the plantbug Nesidiocoris tenuis in tomato crops in southeast Spain. IOBC WPRS Bull 29:243–248

    Google Scholar 

  • Sanchez JA, La Spina MA, Perera OP (2012) Analysis of the population structure of Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae) in the Palaearctic region using microsatellite markers. Ecol Evol 2(12):3145–3159

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanchez JA, del Amor FM, Flores P, López-Gallego E (2015) Nutritional variations at Nesidiocoris tenuis feeding sites and reciprocal interactions between the mirid and tomato plants. J Appl Entomol. doi:10.1111/jen.12246

  • Sasso R, Iodice L, Woodcock CM, Pickett JA, Guerrieri E (2009) Electrophysiological and behavioural responses of Aphidius ervi (Hymenoptera: Braconidae) to tomato plant volatiles. Chemoecology 19(4):195–201

    Article  CAS  Google Scholar 

  • Schuh RT, Slater JA (1995) True bugs of the world. Cornell University Press, Ithaca, New York

    Google Scholar 

  • Silbering AF, Okada R, Ito K, Galizia CG (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075–13087

    Article  CAS  PubMed  Google Scholar 

  • Smith L, Beck JJ (2013) Effect of mechanical damage on emission of volatile organic compounds from plant leaves and implications for evaluation of host plant specificity of prospective biological control agents of weeds. Biocontrol Sci Tech 23(8):880–907

    Article  Google Scholar 

  • Sun X, Liu Z, Zhang A, Dong HB, Zeng FF, Pan XY, Wang Y, Wang MQ (2014) Electrophysiological responses of the rice leaffolder, Cnaphalocrocis medinalis, to rice plant volatiles. J Insect Sci 14(1):70

    Article  PubMed  PubMed Central  Google Scholar 

  • Syntech (2004) Electroantennography: a practical introduction. Hilversum; Netherlands http://www.syntech.nl/manuals/EAGpract.pdf

  • Tavella L, Goula M (2001) Dicyphini collected in horticultural areas of north-western Italy (Heteroptera Miridae). Boll Zool Agric Bach 33(1):93–102

    Google Scholar 

  • Tholl D, Boland W, Hansel A, Loreto F, Röse US, Schnitzler JP (2006) Practical approaches to plant volatile analysis. Plant J 45(4):540–560

    Article  CAS  PubMed  Google Scholar 

  • Tohuara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Ann Rev Physiol 71:307–332

    Article  Google Scholar 

  • Toshova TB, Velchev DI, Subchev MA, Tóth M, Vuts J, Pickett JA, Dewhirst SY (2010) Electrophysiological responses and field attraction of the grey corn weevil, Tanymecus (Episomecus) dilaticollis Gyllenhal (Coleoptera: Curculionidae) to synthetic plant volatiles. Chemoecology 20(3):199–206

    Article  CAS  Google Scholar 

  • Visser JH (1986) Host odor perception in phytophagous insects. Ann Rev Entomol 31:121–144

    Article  Google Scholar 

  • Webster B, Bruce T, Dufour S, Birkemeyer C, Birkett M, Hardie J, Pickett J (2008) Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. J Chem Ecol 34:1153–1161

    Article  CAS  PubMed  Google Scholar 

  • Webster B, Gezan S, Bruce T, Hardie J, Pickett J (2010) Between plant and diurnal variation in quantities and ratios of volatile compounds emitted by Vicia faba plants. Phytochemistry 71:81–89

    Article  CAS  PubMed  Google Scholar 

  • Wheeler AG Jr (2001) Biology of the plant bugs (Hemiptera: Miridae). Cornell University Press, Ithaca, New York

    Google Scholar 

  • Wohlers P, Tjallingii WF (1983) Electroantennogram response of aphids to the alarm pheromone (E)-b-farnesene. Entomol Exp Appl 33:79–82

    Article  CAS  Google Scholar 

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Acknowledgments

Juan Antonio Sánchez was awarded grants by the Ministerio de Ciencia e Innovación (Ramón y Cajal program) and the European Social Fund. Michelangelo La Spina received grants from the INIA. This work was funded in part by the research project PO07-007 (FEDER). We thank two anonymous reviewers for their inspiring comments.

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  1. Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), University of Torino, Largo P. Braccini 2, 10095, Grugliasco, TO, Italy

    B. L. Ingegno & L. Tavella

  2. Instituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA), C/Mayor, 1, La Alberca, 30150, Murcia, Spain

    M. La-Spina, M. J. Jordan & Juan Antonio Sanchez

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  1. B. L. Ingegno
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  2. M. La-Spina
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Correspondence to Juan Antonio Sanchez.

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Ingegno, B.L., La-Spina, M., Jordan, M.J. et al. Host Plant Perception and Selection in the Sibling Species Macrolophus melanotoma and Macrolophus pygmaeus (Hemiptera: Miridae). J Insect Behav 29, 117–142 (2016). https://doi.org/10.1007/s10905-016-9549-1

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