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Exploring the Effects of Plant Odors, from Tree Species of Differing Host Quality, on the Response of Lymantria dispar Males to Female Sex Pheromones

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Abstract

A widely accepted hypothesis for host-plant selection in herbivorous insects is that ovipositing females select host-plants that maximize the survival and performance of their offspring. However, numerous studies indicate that this is not always the case for polyphagous species. Lymantria dispar is a highly polyphagous forest defoliator and has flightless females in some subspecies, resulting in a limited capacity to make host-choices. Males of other Lepidopteran species utilize a combination of sexual pheromones and plant volatiles in their mating choices and exhibit preferences among plant species. We explored the behavior of L. dispar males towards sexual pheromone in the presence and absence of plant volatiles and their ability to discriminate between two plant species with different degrees of suitability for their offspring: a suboptimal host (Pinus sylvestris), and an optimal host (Quercus robur). In no-choice wind tunnel assays, we found that rates of male success in locating a pheromone source were not altered by the presence of plant odors; however, the time spent by males searching for the pheromone source after reaching the full length of the tunnel was reduced by more than 50% in the presence of plant volatiles. In dual choice assays, males exhibited a clear preference for a combination of pheromones and plant volatiles over the pheromone alone. However, we did not find evidence of an innate ability to discriminate between the odors of optimal and suboptimal host plants. We discuss possible ecological and evolutionary explanations for these observations.

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References

  • Adams RP (1995) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publinshing Corp, Carol Stream

    Google Scholar 

  • Allstadt AJ, Haynes KJ, Liebhold AM, Johnson DM (2013) Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect. Oecologia 172:141–151

    Article  PubMed  Google Scholar 

  • Anderson P, Anton S (2014) Experience-based modulation of behavioural responses to plant volatiles and other sensory cues in insect herbivores. Plant Cell Environ 37:1826–1835

    Article  CAS  PubMed  Google Scholar 

  • Anderson P, Sadek M, Larsson M, Hansson B, Thöming G (2013) Larval host plant experience modulates both mate finding and oviposition choice in a moth. Anim Behav 85:1169–1175

    Article  Google Scholar 

  • Badeke E, Haverkamp A, Hansson BS, Sachse S (2016) A challenge for a male noctuid moth? Discerning the female sex pheromone against the background of plant volatiles Front Physiol 7. doi:10.3389/fphys2016.00143

  • Barbosa P, Waldvogel M, Martinat P, Douglass LW (1983) Developmental and reproductive performance of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), on selected hosts common to mid-Atlantic and southern forests. Environ Entomol 12:1858–1862

    Article  Google Scholar 

  • Bell RA, Owens CD, Shapiro M, Tardiff JR (1981) Mass rearing and virus production. In: Doane CC and McManus ML (Eds.), The Gypsy Moth: Research Toward Integrated Pest Management. USDA Forest Service, Technical Bulletin 1584, Washington DC, pp. 599–655

  • Berisford CW, Lanigan TJ, Montgomery ME (1991) Performance of gypsy moth larvae on hosts from the deep south: survival, development and host preferences. In: Gottschalk KW, Twery MJ, smith SI eds. Proceedings, U.S. Department of Agriculture interagency gypsy moth research review 1990. East Windsor, CT. Gen. Tech. Rep. NE-146. Radnor, PA: U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station. p 48

  • Capinera JL, Barbosa P (1976) Dispersal of first-instar gypsy moth larvae in relation to population quality. Oecologia 26:53–60

    Article  PubMed  Google Scholar 

  • Cardé RT, Hagaman TE (1979) Behavioral responses of the gypsy moth in a wind tunnel to air-borne enantiomers of disparlure. Environ Entomol 8:475–484

    Article  Google Scholar 

  • Cardé RT, Knols BGJ (2000) Effects of light levels and plume structure on the orientation manoeuvres of male gypsy moths flying along pheromone plumes. Physiol Entomol 25:141–150

    Article  Google Scholar 

  • Cardé R, Doane C, Baker T, Iwaki S, Marumo S (1977) Attractancy of optically active pheromone for male gypsy moths. Environ Entomol 6:768–772

    Article  Google Scholar 

  • Charlton RE, Cardé RT (1982) Rate and diel periodicity of pheromone emission from female gypsy moths, (Lymantria dispar) determined with a glass-adsorption collection system. J Insect Physiol 28:423–430

    Article  Google Scholar 

  • Charlton R, Cardé R (1990a) Factors mediating copulatory behavior and close-range mate recognition in the male gypsy moth. Lymantria dispar (L) Can J Zool 68:1995–2004

  • Charlton RE, Cardé RT (1990b) Orientation of male gypsy moths, Lymantria dispar (L.), to pheromone sources: the role of olfactory and visual cues. J Insect Behav 3:443–469

    Article  Google Scholar 

  • Charlton RE, Kanno H, Collins RD, Carde RT (1993) Influence of pheromone dose and ambient temperature on flight of the gypsy moth, Lymantria dispar (L), in a sustained-flight wind tunnel. Physiol Entomol 18:349–362

    Article  CAS  Google Scholar 

  • Choi H-S (2003) Character impact odorants of citrus hallabong [(C. Unshiu Marcov x C. sinensis Osbeck) x C. reticulata Blanco] cold-pressed peel oil. J Agric Food Chem 51:2687–2692

    Article  CAS  PubMed  Google Scholar 

  • Deisig N, Dupuy F, Anton S, Renou M (2014) Responses to pheromones in a complex odor world: sensory processing and behavior. Insects 5:399–422

    Article  PubMed  PubMed Central  Google Scholar 

  • Dickens JC, Smith JW, Light DM (1993) Green leaf volatiles enhance sex attractant pheromone of the tobacco budworm, Heliothis virescens (Lep.: Noctuidae). Chemoecology 4:175–177

    Article  CAS  Google Scholar 

  • Emelianov I, Drès M, Baltensweiler W, Mallet J (2001) Host-induced assortative mating in host races of the larch budmoth. Evolution 55:2002–2010

    Article  CAS  PubMed  Google Scholar 

  • Erelli MC, Elkinton JS (2000) Factors influencing dispersal in neonate gypsy moths (Lepidoptera: Lymantriidae). Environ Entomol 29:509–515

    Article  Google Scholar 

  • Félix A-E, Smaïl T, Frérot B (2013) Host plants and reproductive behaviour in the African maize stemborer, Busseola fusca (Fuller 1901)(Lepidoptera: Noctuidae). In: Annales de la Société Entomologique de France, 2013. vol 1. Taylor & Francis, pp 68–72

  • Forbush EH, Fernald CH (1896) The gypsy moth: Porthetria dispar (Linn.). A report of the work of destroying the insect in the commonwealth of Massachusetts, together with an account of its history and habits both in Massachusetts and Europe. Boston, USA

  • Foster JR, Townsend PA, Mladenoff DJ (2013) Spatial dynamics of a gypsy moth defoliation outbreak and dependence on habitat characteristics. Landscape Ecol 28:1307–1320

    Article  Google Scholar 

  • Friberg M, Olofsson M, Berger D, Karlsson B, Wiklund C (2008) Habitat choice precedes host plant choice–niche separation in a species pair of a generalist and a specialist butterfly. Oikos 117:1337–1344

    Article  Google Scholar 

  • Friberg M, Posledovich D, Wiklund C (2015) Decoupling of female host plant preference and offspring performance in relative specialist and generalist butterflies. Oecologia 178:1181–1192

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Robledo C, Horvitz CC (2012) Parent-offspring conflicts, "optimal bad motherhood" and the "mother knows best" principles in insect herbivores colonizing novel host plants. Ecol Evol 2:1446–1457

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong Y, Plettner E (2011) Effects of Aromatic Compounds on Antennal Responses and on the Pheromone-Binding Proteins of the Gypsy Moth (Lymantria dispar) Chem Senses 36:291–300

  • Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecol Lett 13:383–393

    Article  PubMed  Google Scholar 

  • Hamm S, Bleton J, Connan J, Tchapla A (2005) A chemical investigation by headspace SPMS and GC-MS of volatile and semi-volatile terpenes in various olibanum samples. Phytochem 66:1499–1514

    Article  CAS  Google Scholar 

  • Higashiura Y (1989a) Survival of eggs in the gypsy-moth Lymantria-dispar I. Predation by birds. J Anim Ecol 58:403–412

    Article  Google Scholar 

  • Higashiura Y (1989b) Survival of eggs in the gypsy moth Lymantria dispar II. Oviposition site selection in changing environments. J Anim Ecol 58:413–426

    Article  Google Scholar 

  • Högnadottir A, Rouseff RL (2003) Identification of aroma active compounds in orange essence oil using gas chromatography – olfactometry and gas chromatography - mass spectrometry. J Chromatogr A 998:201–211

    Article  PubMed  Google Scholar 

  • Jactel H, Birgersson G, Andersson S, Schlyter F (2011) Non-host volatiles mediate associational resistance to the pine processionary moth. Oecologia 166:703–711

    Article  CAS  PubMed  Google Scholar 

  • Jaenike J (1978) On optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356

    Article  CAS  PubMed  Google Scholar 

  • Karioti A, Skaltsa H, Demetzos C, Perdetzoglou D, Economakis CD, Salem AB (2003) Effects of nitrogen concentration of the nutrient solution on the volatile constiuents of leaves of Salvia fruticosa mill. In solution culture J Agric Food Chem 51:6505–6508

    Article  CAS  PubMed  Google Scholar 

  • Keeler MS, Chew FS (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568

    Article  PubMed  Google Scholar 

  • Keena MA, Cote MJ, Grinberg PS, Wallner WE (2008) World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environ Entomol 37:636–649

    Article  CAS  PubMed  Google Scholar 

  • Lance D, Barbosa P (1981) Host tree influences on the dispersal of first instar gypsy moths. Lymantria dispar (L) Ecol Entomol 6:411–416

  • Leonard DE (1981) Bioecology of the gypsy moth. In: Doane TCC, McManus ML (eds) The Gypsy Moth: Research toward Integrated Pest Management,. U.S. Department of Agriculture, Washington D.C., USA, pp 9–30

  • Li J, VAlimaki S, Shi J, Zong S, Luo Y (2012) Attraction of the gypsy moth to volatile organic compounds (VOCs) of damaged Dahurian larch. Z Naturforsch 67:437–444

    Article  CAS  Google Scholar 

  • Light DM, Flath RA, Buttery RG, Zalom FG, Rice RE, Dickens JC, Jang EB (1993) Host-plant green-leaf volatiles synergize the synthetic sex pheromones of the corn earworm and codling moth (Lepidoptera). Chemoecology 4:145–152

    Article  CAS  Google Scholar 

  • Liu Z, Li D, Gong P, Wu K (2004) Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different host plants. Environ Entomol 33:1570–1576

    Article  Google Scholar 

  • Löfstedt C, Linn CE, Löfqvist J (1985) Behavioral responses of male turnip moths, Agrotis segetum, to sex pheromone in a flight tunnel and in the field. J Chem Ecol 11:1209–1221

    Article  PubMed  Google Scholar 

  • Maja MM, Kasurinen A, Holopainen T, Kontunen-Soppela S, Oksanen E, Holopainen JK (2015) Volatile organic compounds emitted from silver birch of different provenances across a latitudinal gradient. Finland Tree Physiol 35:975–986

    Article  PubMed  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • McCormick AC, Karlsson M, Bosa-Ochoa CF, Proffit M, Bengtsson M, Zualuaga MV, Fukumoto T, Oehlschlager C, Cotes-Prado AM, Witzgall P (2012) Mating disruption of Guatemalan potato moth Tecia Solanivora by attractive and non-attractive pheromone blends. J Chem Ecol 38:63–70

    Article  PubMed  Google Scholar 

  • McCormick AC, Irmisch S, Reinecke A, Boeckler GA, Veit D, Reichelt M, Hansson BS, Gershenzon J, Köllner TG, Unsicker SB (2014) Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37:1909–1923

    Article  Google Scholar 

  • McCormick AC, Reinecke A, Gershenzon J, Unsicker SB (2016) Feeding Experience Affects the Behavioral Response of Polyphagous Gypsy Moth Caterpillars to Herbivore-induced Poplar Volatiles. J Chem Ecol 1–12 doi:10.1007/s10886-016-0698-7

  • Montgomery ME (1991) Variation in the suitability of tree species for the gypsy moth. Gypsy Moth Research Review 13 Pp. In: Gottschalk KW, Twery MJ, Smith SI Eds. Proceedings, U.S. Department of Agriculture interagency gypsy moth research review 1990. East Windsor, CT. Gen. Tech. Rep. NE-146. Radnor, PA: U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station: pp 1–13

  • Mozaffar A (2013) Biogenic volatile organic compound emissions from willow trees. Master degree project in physical geography and ecosystem analysis. Lund University, Sweden

    Google Scholar 

  • Plettner E, Gries R (2010) Agonists and antagonists of antennal responses of gypsy moth (Lymantria dispar) to the pheromone (+)-disparlure and other odorants. J Agric Food Chem 58:3708–3719

    Article  CAS  PubMed  Google Scholar 

  • Pogue MG, Schaeffer PW (2007) A review of selected species of Lymantria (Hubner, 1819.) US Department of Agriculture (USDA), Washington DC, USA.

  • Proffit M, Khallaf MA, Carrasco D, Larsson MC, Anderson P (2015) ‘do you remember the first time?‘host plant preference in a moth is modulated by experiences during larval feeding and adult mating. Ecol Lett 18:365–374

    Article  PubMed  Google Scholar 

  • Rausher MD (1979) Larval habitat suitability and oviposition preference in three related butterflies. Ecology 503–511

  • Reddy G, Guerrero A (2000) Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp. capitata. J Agric Food Chem 48:6025–6029

    Article  CAS  PubMed  Google Scholar 

  • Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261

    Article  CAS  PubMed  Google Scholar 

  • Renwick J, Chew F (1994) Oviposition behavior in Lepidoptera. Annu Rev Entomol 39:377–400

    Article  Google Scholar 

  • Schmidt-Büsser D, Von Arx M, Guerin PM (2009) Host plant volatiles serve to increase the response of male European grape berry moths, Eupoecilia ambiguella, to their sex pheromone. J Comp Physiol 195:853–864

    Article  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, Oxford, UK

    Google Scholar 

  • Schweitzer DF (2004) Gypsy moth (Lymantria dispar): impacts and options for biodiversity-oriented land managers. NatureServ, Arlington, Virginia, 59 Pp

    Google Scholar 

  • Shields VDC, Broomell BP, Salako JOB (2003) Host selection and acceptability of selected tree species by gypsy moth larvae. Lymantria dispar (L) Ann Entomol Soc Am 96:920–926

  • Thöming G, Larsson MC, Hansson BS, Anderson P (2013) Comparison of plant preference hierarchies of male and female moths and the impact of larval rearing hosts. Ecology 94:1744–1752

    Article  PubMed  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89

    Article  Google Scholar 

  • Tobin PC, Klein KT, Leonard DS (2009) Gypsy moth (Lepidoptera: Lymantriidae) flight behavior and phenology based on field-deployed automated pheromone-baited traps. Environ Entomol 38:1555–1562

    Article  PubMed  Google Scholar 

  • Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos BE, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10:255–271

    Article  CAS  Google Scholar 

  • Valim MF, Rouseff RL, Lin J (2003) Gas chromatographic-olfactometric characterization of aroma compounds in two types of cashew apple nectar. J Agric Food Chem 51:1010–1015

    Article  CAS  PubMed  Google Scholar 

  • Varela N, Avilla J, Anton S, Gemeno C (2011) Synergism of pheromone and host-plant volatile blends in the attraction of Grapholita molesta males. Entomol Exp Appl 141:114–122

    Article  CAS  Google Scholar 

  • Von Arx M, Schmidt-Büsser D, Guerin PM (2012) Plant volatiles enhance behavioral responses of grapevine moth males, Lobesia botrana to sex pheromone. J Chem Ecol 38:222–225

    Article  PubMed  Google Scholar 

  • Wainhouse D (2005) Ecological methods in forest pest management. Oxford university press on demand. UK, Oxford, 227 Pp

    Google Scholar 

  • Wiklund C (1974) Oviposition preferences in Papilio machaon in relation to the host plants of the larvae. Entomol Exp Appl 17:189–198

    Article  Google Scholar 

  • Wiklund C, Friberg M (2009) The evolutionary ecology of generalization: among-year variation in host plant use and offspring survival in a butterfly. Ecology 90:3406–3417

    Article  PubMed  Google Scholar 

  • Willis MA, Cardé RT (1990) Pheromone-modulated optomotor response in male gypsy moths, Lymantria dispar L.: upwind flight in a pheromone plume in different wind velocities. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 167:699–706

    Article  Google Scholar 

  • Yang Z, Bengtsson M, Witzgall P (2004) Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella pheromone. J Chem Ecol 30:619–629

    Article  CAS  PubMed  Google Scholar 

  • Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Ann Rev of Entomol 47:361–393

    Article  CAS  Google Scholar 

  • Zhang A (2005) Laboratory evaluation of semiochemical dispensers: a Theoretical chemical kinetic approach to the emission rate of disparlure active ingredient. Paper presented at the 16th US Department of Agriculture Interagency Research Forum on Gypsy Moth and Other Invasive Species., Delaware, US

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Acknowledgements

The authors would like to acknowledge all members of the Biocommunication and Ecology lab at ETH Zurich for their support and collaboration. This project was possible thanks to the funding provided to Andrea Clavijo McCormick by the International Post-doctoral Fellowship Program in Plant Science -Plant Fellows- A Marie Curie initiative managed by the Zurich-Basel Plant Science Center.

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  1. ETH Zürich, Department of Environmental Systems Science, Schmelzbergstarsse 9, 8092, Zürich, Switzerland

    Andrea Clavijo McCormick, Jonathan Heyer, James W. Sims, Mark C. Mescher & Consuelo M. De Moraes

  2. Institute of Agriculture and Environment, Massey University, Private Bag 11222, Palmerston North, 4442, New Zealand

    Andrea Clavijo McCormick

  3. Kantonaler Pflanzenschutzdienst, Landwirtschaftliches Institut des Kantons Freiburg, Route de Grangeneuve, 311725, Posieux, Switzerland

    Jonathan Heyer

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  1. Andrea Clavijo McCormick
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McCormick, A.C., Heyer, J., Sims, J.W. et al. Exploring the Effects of Plant Odors, from Tree Species of Differing Host Quality, on the Response of Lymantria dispar Males to Female Sex Pheromones. J Chem Ecol 43, 243–253 (2017). https://doi.org/10.1007/s10886-017-0825-0

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