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Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment

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Abstract

In weed biological control programs, pre-release host-specificity testing relies traditionally on no-choice and choice feeding, oviposition, and development tests. Rarely have they included detailed examination of behavioral responses to olfactory and visual cues of biological control candidates, although a better understanding of the mechanisms underlying host recognition may explain potential discrepancies between choice and no-choice tests, and/or between tests conducted in the lab versus field conditions. We investigated how the seed-feeding weevil, Mogulones borraginis, distinguishes its host plant, Cynoglossum officinale, from three native confamilial non-target species in North America. In behavioral bioassays, M. borraginis responded to olfactory and visual cues individually and, to an even greater extent, to both plant cue modalities when offered simultaneously. In tests with the combined cues, M. borraginis was attracted to C. officinale but responded with indifference or was repelled by non-target plants. In electrophysiological experiments, we identified that M. borraginis responded to ten volatile compounds and four wavelengths of lights from inflorescences of C. officinale. We propose that studies of responses to multimodal plant cues can advance our understanding of how biocontrol candidate species discriminate among host plants and closely related non-target species, thereby increasing the accuracy of environmental safety assessments pre-release.

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References

  • Andreas JE, Schwarzländer M, Ding H, Eigenbrode SD (2009) Post-release non-target monitoring of Mogulones cruciger, a biological control agent released to control Cynoglossum officinale in Canada. In: Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, Hinz HL, Rector BG (eds) Proceedings of the 12th international symposium on biological control of weeds. CAB International, Wallingford, United Kingdom, pp 75–82

    Google Scholar 

  • Balkenius A, Bisch-Knaden S, Hansson B (2009) Interaction of visual and odour cues in the mushroom body of the hawkmoth Manduca sexta. J Exp Biol 212:535–541

    Article  PubMed  Google Scholar 

  • Briese DT (2005) Translating host-specificity test results into the real world: the need to harmonize the yin and yang of current testing procedures. Biol Control 35:208–214

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Catton HA, Lalonde RG, De Clerck-Floate RA (2014) Differential host-finding abilities by a weed biocontrol insect create within-patch spatial refuges for nontarget plants. Environ Entomol 43:1333–1344

    Article  PubMed  Google Scholar 

  • Cohen JI (2015) Adelinia and Andersonglossum (Boraginaceae), two new genera from new world species of Cynoglossum. Syst Bot 40:611–619

    Article  Google Scholar 

  • Cosse AA, Bartelt RJ, Zilkowski BW, Bean DW, Andress ER (2006) Behaviorally active green leaf volatiles for monitoring the leaf beetle, Diorhabda elongata, a biocontrol agent of saltcedar, Tamarix spp. J Chem Ecol 32:2695–2708

    Article  PubMed  CAS  Google Scholar 

  • Crook DJ, Francese JA, Zylstra KE, Fraser I, Sawyer AJ, Bartels DW, Lance DR, Mastro VC (2009) Laboratory and field response of the emerald ash borer (Coleoptera: Buprestidae), to selected regions of the electromagnetic spectrum. J Econ Entomol 102:2160–2169

    Article  PubMed  Google Scholar 

  • de Jong TJ, Klinkhamer PGL, Prins AH (1986) Flowering behaviour of the monocarpic perennial Cynoglossum officinale (L.). New Phytol 103:219–229

    Article  Google Scholar 

  • Degen T, Städler E (1997) Foliar form, colour and surface characteristics influence oviposition behaviour of the carrot fly Entomol Exp Appl 83:99–112

  • Dekker T, Ignell R, Ghebru M, Glinwood R, Hopkins R (2011) Identification of mosquito repellent odours from Ocimum forskolei. Parasites Vectors 4:183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farkas SR, Shorey HH (1972) Chemical trail-following by flying insects: a mechanism for orientation to a distant odor source. Science 178:67–68

    Article  PubMed  CAS  Google Scholar 

  • Flath R, Cunningham R, Mon T, John J (1994) Male lures for Mediterranean fruitfly (Ceratitis capitata Wied.): structural analogs of α-copaene. J Chem Ecol 20:2595–2609

    Article  PubMed  CAS  Google Scholar 

  • Francis F, Lognay G, Haubruge E (2004) Olfactory responses to aphid and host plant volatile releases:(E)-β-farnesene an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741–755

    Article  PubMed  CAS  Google Scholar 

  • Graziosi I, Rieske LK (2013) Response of Torymus sinensis, a parasitoid of the gallforming Dryocosmus kuriphilus, to olfactory and visual cues. Biol Control 67:137–142

    Article  Google Scholar 

  • Harris MO, Foster SP (1995) Behavior and integration. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects 2. Springer, Boston, pp 3–46

    Chapter  Google Scholar 

  • Harris M, Miller J (1982) Synergism of visual and chemical stimuli in the oviposition behaviour of Delia antiqua. In: Visser JH, Minks AK (eds) 5th international symposium on insect-plant relationships, Wageningen, Netherlands, 1982. Centre for Agricultural Publishing and Documentation, pp 117–122

  • Heard TA (2000) Concepts in insect host-plant selection behavior and their application to host specificity testing. In: van Driesche RG, Heard T, McClay A, Reardon R (eds) Proceedings: host specificity testing of exotic arthropod biological control agents: the biological basis for improvement in safety. US Forest Service, Forest Health Technology Enterpirse Team, Morgantown, Wester Virginia, pp 1–10

  • Hinz HL, Cripps M, Hugli D, Medina K, Meyer S, Tosevski I (2003) Biological control of houndstongue, Cynoglossum officinale, Annual Report 2002. CABI Bioscience Switzerland Centre, Delemont

    Google Scholar 

  • Hinz HL, Bartels L, Tosevski I (2004) Biological control of houndstongue Cynoglossum officinale, Annual Report 2003. CABI Bioscience Switzerland Centre, Delemont

    Google Scholar 

  • Hinz HL, Bilat J, Svejcar L, Schwarzländer M, Harverhals M, Bruns M, Cole M, Harmon B (2010) Host-specificity tests conducted with Mogulones borraginis in 2009. CABI Bioscience Switzerland Centre, Delemont

    Google Scholar 

  • Hinz HL, Schwarzländer M, Gassmann A, Bourchier RS (2014) Successes we may not have had: a retrospective analysis of selected weed biological control agents in the United States. Invas Plant Sci Mana 7:565–579

    Article  CAS  Google Scholar 

  • Kafle B (2016) Olfaction mediated host selection in a specialist weevil used for biological control of an invasive plant. Master thesis, University of Idaho

  • Knolhoff LM, Heckel DG (2014) Behavioral assays for studies of host plant choice and adaptation in herbivorous insects. Annu Rev Entomol 59:263–278

    Article  PubMed  CAS  Google Scholar 

  • Koch K (1992) Die Käfer Mitteleuropas, Ökologie. In: Freude H, Harde KW, Lohse GA (eds), vol 3. Goecke & Evers Verlag, Krefeld, Germany, p 111

  • Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396

    Article  PubMed  CAS  Google Scholar 

  • Marohasy J (1998) The design and interpretation of host-specificity tests for weed biological control with particular reference to insect behavior. Biocontrol News Inf 19:13–20

    Google Scholar 

  • McCormick AC, Gershenzon J, Unsicker SB (2014) Little peaks with big effects: establishing the role of minor plant volatiles in plant-insect interactions. Plant, Cell Environ 37:1836–1844

    Article  Google Scholar 

  • Milet-Pinheiro P, Ayasse M, Dotterl S (2015) Visual and olfactory floral cues of Campanula (Campanulaceae) and their significance for host recognition by an oligolectic bee pollinator. PLoS ONE 10(6):e0128577

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller JR, Strickler KL (1984) Finding and accepting host plants. In: Bell WJ, Carde RT (eds) Chemical ecology of insects. Sinauer Associates, Boston, pp 127–157

    Chapter  Google Scholar 

  • Müller E, Nentwig W (2011) How to find a needle in a haystack - host plant finding of the weevil Ceratapion onopordi. Entomol Exp Appl 139:68–74

    Article  Google Scholar 

  • Park I (2017) The role of olfactory and visual cues in the host finding behavior of a near-monophagous specialist insect herbivore considered for biological control of weeds. PhD dissertation, University of Idaho

  • Peterson ML, Miller TJ, Kay KM (2015) An ultraviolet floral polymorphism associated with life history drives pollinator discrimination in Mimulus Guttatus. Am J Bot 102:396–406

    Article  PubMed  Google Scholar 

  • Reeves JL, Lorch PD (2009) Visual plant differentiation by the milfoil weevil, Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae). J Insect Behav 22:473–476

    Article  Google Scholar 

  • Reeves JL, Lorch PD (2011) Visual active space of the milfoil weevil, Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae). J Insect Behav 24:264–273

    Article  Google Scholar 

  • Reeves J, Lorch P, Kershner M (2009) Vision is important for plant location by the phytophagous aquatic specialist Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae). J Insect Behav 22:54–64

    Article  Google Scholar 

  • SAS Institute (2015) Base SAS 9.4 Procedures Guide. SAS Institute, Cary, North Carolina, United States of America

  • Schaffner U (2001) Host range testing of insects for biological weed control: how can it be better interpreted? BioScience 51:1–9

    Article  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology Ed. 2. Oxford University Press, Oxford

  • Sheppard AW, van Klinken RD, Heard TA (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215–226

    Article  Google Scholar 

  • Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9(1):e84847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tooker JF, Crumrin AL, Hanks LM (2005) Plant volatiles are behavioral cues for adult females of the gall wasp Antistrophus rufus. Chemoecology 15:85–88

    Article  CAS  Google Scholar 

  • Upadhyaya MK, Tilsner HR, Pitt MD (1988) The biology of canadian weeds. 87. Cynoglossum officinale L. Can J Plant Sci 68:763–774

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Weiss MR (1991) Floral color changes as cues for pollinators. Nature 354:227–229

    Article  Google Scholar 

  • Wheeler GS, Schaffner U (2013) Improved understanding of weed biological control safety and impact with chemical ecology: a review. Invas Plant Sci Mana 6:16–29

    Article  CAS  Google Scholar 

  • Williams JL (2009) Flowering life-history strategies differ between the native and introduced ranges of a monocarpic perennial. Am Nat 174:660–672

    Article  PubMed  Google Scholar 

  • Winston R, Schwarzländer M, Hinz HL, Day MD, Cock MJ, Julien M (2014) Biological control of weeds: a world catalogue of agents and their target weeds. 5th edn. USDA Forest Service, Forest Health Techonology Enterprise Team, Morgantown, West Virginia

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Acknowledgements

We thank Richard Reardon for his ongoing support of this research, Karen Humes for loan of the GER 2600 photo-radiometer, Aaron Stancik for constructing the electroretinography instrument, Ying Wu for maintaining the GC-MS instruments, and Bill Price for his assistance with statistical analysis. This research was funded by USDI Bureau of Land Management CESU Agreement HAA0807402 and USDA Forest Service Cooperative Agreement 10-CA-11420004 to M.S.

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Authors and Affiliations

  1. Department of Entomology, Plant Pathology and Nematology, University of Idaho, 875 Perimeter Drive, MS 2339, Moscow, ID, 83844-2339, USA

    Ikju Park, Sanford D. Eigenbrode, Stephen P. Cook, Bradley L. Harmon & Mark Schwarzländer

  2. CABI, Rue des Grillons 1, 2800, Delémont, Switzerland

    Hariet L. Hinz & Urs Schaffner

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  1. Ikju Park
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  2. Sanford D. Eigenbrode
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  3. Stephen P. Cook
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  4. Bradley L. Harmon
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  5. Hariet L. Hinz
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  6. Urs Schaffner
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  7. Mark Schwarzländer
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Correspondence to Ikju Park.

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Handling Editor: Mark Schwarzländer, Cliff Moran and S. Raghu.

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Park, I., Eigenbrode, S.D., Cook, S.P. et al. Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment. BioControl 63, 377–389 (2018). https://doi.org/10.1007/s10526-018-9867-7

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  • DOI: https://doi.org/10.1007/s10526-018-9867-7

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