Skip to main content
SpringerLink
Log in

Chemically Mediated Host-Plant Selection by the Milfoil Weevil: A Freshwater Insect–Plant Interaction

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The milfoil weevil Euhrychiopsis lecontei is a specialist aquatic herbivore that feeds, oviposits, and mates on the invasive freshwater macrophyte Myriophyllum spicatum. We characterized the weevil's preference for M. spicatum, and through bioassay-driven fractionation, isolated and identified two chemicals released by M. spicatum that attract E. lecontei. Mass spectrometry and nuclear magnetic resonance spectroscopy were used to identify the attractive compounds as glycerol and uracil. Dose-response curves for glycerol and uracil indicated that weevil preference increased as sample concentration increased. Weevils were attracted to a crude sample of M. spicatum-released chemicals from 0.17 to 17 mg/l, to glycerol from 18 to 1800 μM (0.0017–0.17 mg/l), and to uracil from 0.015 to 15 μM (0.00014–1.4 mg/l). Although glycerol and uracil are ubiquitous, weevils are likely responding to high concentrations that are released as a result of the rapid growth of M. spicatum. Uracil concentration was greater in the exudates of M.spicatum than other Myriophyllum spp. E. lecontei was attracted to glycerol at a concentration similar to that at which terrestrial insects are attracted to sugar alcohols. This is the first example of a freshwater specialist insect being attracted to chemicals released by its host plant. Analysis of the water milfoil–weevil interaction provides further understanding as to how insects locate their host plants in aquatic systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • E. Bartlet M. M. Blight P. Lane I. H. Williams (1997) ArticleTitleThe responses of the cabbage seed weevil Ceutorhynchus assimilis to volatile compounds from oilseed rape in a linear track olfactometer Entomol. Exp. Appl. 85 257–262 Occurrence Handle10.1023/A:1003140219888

    Article  Google Scholar 

  • E. A. Bernays R. F. Chapman (1994) Host Plant Selection by Phytophagous Insects Chapman & Hall New York

    Google Scholar 

  • C. W. Boylen L. W. Eichler J. D. Madsen (1999) ArticleTitleLoss of native aquatic plant species in a community dominated by Eurasian watermilfoil Hydrobiologia 415 207–211 Occurrence Handle10.1023/A:1003804612998

    Article  Google Scholar 

  • E. G. Brown Y. Turan (1995) ArticleTitlePyrimidine metabolism and secondary product formation; biogenesis of albizziine, 4-hydroxyhomoarginine and 2,3-diaminopropanoic acid Phytochemistry 40 763–771 Occurrence Handle10.1016/0031-9422(95)00317-Z Occurrence Handle1:CAS:528:DyaK2MXoslyksLc%3D

    Article  CAS  Google Scholar 

  • T. J. A. Bruce L. J. Wadhams C. M. Woodcock (2005) ArticleTitleInsect host location: a volatile situation Trends Plant Sci. 10 269–274 Occurrence Handle15949760 Occurrence Handle10.1016/j.tplants.2005.04.003 Occurrence Handle1:CAS:528:DC%2BD2MXltVaqsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • G. R. Buckingham C. A. Bennett (1995) ArticleTitleHost range studies with Bagous affinis (Coleoptera: Curculionidae), an Indian weevil that feeds on hydrilla tubers Environ. Entomol. 27 469–479

    Google Scholar 

  • W. E. S. Carr (1988) The molecular nature of chemical stimuli in the aquatic environment J. Atema R. R. Fay A. N. Popper W. N. Tavolga (Eds) Sensory Biology of Aquatic Animals Springer-Verlag New York 3–27

    Google Scholar 

  • T. D. Center F. A. Dray G. Jubinsky M. J. Grodowitz (2002) Insects and Other Arthropods that Feed on Aquatic and Wetland Plants USDA, Agricultural Research Service Fort Lauderdale, FL

    Google Scholar 

  • R. F. Chapman (2003) ArticleTitleContact chemoreception in feeding by phytophagous insects Annu. Rev. Entomol. 48 455–484 Occurrence Handle12414737 Occurrence Handle10.1146/annurev.ento.48.091801.112629 Occurrence Handle1:CAS:528:DC%2BD3sXnvVyksg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C. Choi C. Bareiss O. Walenciak E. M. Gross (2002) ArticleTitleImpact of polyphenols on growth of the aquatic herbivore Acentria ephemerella J. Chem. Ecol. 28 2245–2256 Occurrence Handle12523565 Occurrence Handle10.1023/A:1021049332410 Occurrence Handle1:CAS:528:DC%2BD38Xos1Knur4%3D

    Article  PubMed  CAS  Google Scholar 

  • R. P. Creed S. P. Sheldon (1994) ArticleTitleAquatic weevils (Coleoptera, Curculionidae) associated withnorthern watermilfoil (Myriophyllum sibiricum) in Alberta, Canada Entomol. News 105 98–102

    Google Scholar 

  • R. P. Creed S. P. Sheldon (1995) ArticleTitleWeevils and watermilfoil: Did a North American herbivore cause the decline of an exotic plant? Ecol. Appl. 5 1113–1121

    Google Scholar 

  • G. Cronin K. D. Wissing D. M. Lodge (1998) ArticleTitleComparative feeding selectivity of herbivorous insects on water lilies: aquatic vs. semi-terrestrial insects and submersed vs. floating leaves Freshw. Biol. 39 243–257 Occurrence Handle10.1046/j.1365-2427.1998.00279.x

    Article  Google Scholar 

  • G. Cronin D. M. Lodge M. E. Hay M. Miller A. M. Hill T. Horvath R. C. Bolser N. Lindquist M. Wahl (2002) ArticleTitleCrayfish feeding preferences for fresh water macrophytes: The influence of plant structure and chemistry J. Crustac. Biol. 22 708–718

    Google Scholar 

  • A. W. Decho K. A. Browne R. K. Zimmerfaust (1998) ArticleTitleChemical cues: Why basic peptides are signal molecules in marine environments Limnol. Oceanogr. 43 1410–1417 Occurrence Handle1:CAS:528:DyaK1MXkvVym Occurrence Handle10.4319/lo.1998.43.7.1410

    Article  CAS  Google Scholar 

  • P. J. Eastmond (2004) ArticleTitleGlycerol-insensitive Arabidopsis mutants: Gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress Plant J. 37 617–625 Occurrence Handle14756771 Occurrence Handle10.1111/j.1365-313X.2003.01989.x Occurrence Handle1:CAS:528:DC%2BD2cXisVWhtr8%3D

    Article  PubMed  CAS  Google Scholar 

  • D. W. Gerber R. U. Byerrum R. W. Gee N. E. Tolbert (1988) ArticleTitleGlycerol concentration in crop plants Plant Sci. 56 31–38 Occurrence Handle10.1016/0168-9452(88)90182-3 Occurrence Handle1:CAS:528:DyaL1cXmtVygsbY%3D

    Article  CAS  Google Scholar 

  • H. Godmaire C. Nalewajko (1990) ArticleTitleStructure and development of secretory trichomes on Myriophyllum spicatum L Aquat. Bot. 37 99–121 Occurrence Handle10.1016/0304-3770(90)90085-Y

    Article  Google Scholar 

  • E. M. Gross (2003) ArticleTitleDifferential response of tellimagrandin II and total bioactive hydrolysable tannins in an aquatic angiosperm to changes in light and nitrogen Oikos 103 497–504 Occurrence Handle10.1034/j.1600-0706.2003.12666.x Occurrence Handle1:CAS:528:DC%2BD3sXpvFCiurg%3D

    Article  CAS  Google Scholar 

  • E. M. Gross H. Meyer G. Schilling (1996) ArticleTitleRelease and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum Phytochemistry 41 133–138 Occurrence Handle10.1016/0031-9422(95)00598-6 Occurrence Handle1:CAS:528:DyaK28XisVWqsA%3D%3D

    Article  CAS  Google Scholar 

  • M. E. Hay P. D. Steinberg (1992) The chemical ecology of plant–herbivore interactions in marine versus terrestrial communities G. A. Rosenthal M. R. Berenbaum (Eds) Herbivores: Their Interactions with Secondary Plant Metabolites, 2E Academic Press San Diego, CA 371–413

    Google Scholar 

  • M. E. Hay J. J. Stachowicz E. Cruz-Rivera S. Bullard M. S. Deal N. Lindquist (1998) Bioassays with marine and freshwater macroorganisms K. F. Haynes J. G. Millar (Eds) Methods in Chemical Ecology, Vol. 2, Bioassay Methods Chapman and Hall New York 39–141

    Google Scholar 

  • J. Kubanek M. E. Hay P. J. Brown N. Lindquist W. Fenical (2001) ArticleTitleLignoid chemical defenses in the freshwater macrophyte Saururus cernuus Chemoecology 11 1–8 Occurrence Handle1:CAS:528:DC%2BD3MXivVOkurk%3D

    CAS  Google Scholar 

  • E. Leu A. Krieger-Liszkay C. Goussias E. M. Gross (2002) ArticleTitlePolyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II Plant Physiol. 130 2011–2018 Occurrence Handle12481084 Occurrence Handle10.1104/pp.011593 Occurrence Handle1:CAS:528:DC%2BD3sXktlOh

    Article  PubMed  CAS  Google Scholar 

  • Y. K. Li D. Yu X. Yan (2004) ArticleTitleAre polyphenolics valuable in anti-herbivory strategies of submersed freshwater macrophytes? Arch. Hydrobiol. 161 391–402 Occurrence Handle10.1127/0003-9136/2004/0161-0391 Occurrence Handle1:CAS:528:DC%2BD2MXht1Kkt78%3D

    Article  CAS  Google Scholar 

  • H. Lyr H. Streitberg (1955) ArticleTitleDie Verbreitung von Hydropoten in verschiedenen Verwandtschaftskreisen der Wasserpflanzen Wiss. Z.–Martin-Luther-Univ. Halle-Wittenb., Math.-Nat.Wiss. Reihe 4 471–484

    Google Scholar 

  • J. D. Madsen C. F. Hartleb C. W. Boylen (1991) ArticleTitlePhotosynthetic characteristics of Myriophyllum spicatum and six submersed aquatic macrophyte species native to Lake George, New York Freshw. Biol. 26 233–240

    Google Scholar 

  • M. D. Marko F. R. Stermitz (1997) ArticleTitleTransfer of alkaloids from Delphinium to Castilleja via root parasitism. Norditerpenoid alkaloid analysis by electrospray mass spectrometry Biochem. Syst. Ecol. 25 279–285 Occurrence Handle1:CAS:528:DyaK2sXksVGmtLw%3D Occurrence Handle10.1016/S0305-1978(97)00010-0

    Article  CAS  Google Scholar 

  • B. Meijkamp R. Aerts J. Staaij ParticleVan De M. Tosserams W. H. O. Ernst J. Rozema (1999) Effects of UV-B on secondary metabolites in plants J. Rozema (Eds) Stratospheric Ozone Depletion: The Effects of Enhanced UV-B Radiation on Terrestrial Ecosystems Backhuys Publishers Leiden, The Netherlands 71–99

    Google Scholar 

  • R. L. Metcalf E. R. Metcalf (1992) Chemical Ecology of Plant Kairomones Chapman and Hall New York, NY

    Google Scholar 

  • M. L. Moody D. H. Les (2002) ArticleTitleEvidence of hybridity in invasive watermilfoil (Myriophyllum) populations Proc. Natl. Acad. Sci. USA 99 14867–14871 Occurrence Handle12407174 Occurrence Handle10.1073/pnas.172391499 Occurrence Handle1:CAS:528:DC%2BD38Xpt1yrt7s%3D

    Article  PubMed  CAS  Google Scholar 

  • S. Nakai Y. Inoue A. Hosomi A. Murakami (2000) ArticleTitleMyriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa Water Res. 34 3026–3032 Occurrence Handle10.1016/S0043-1354(00)00039-7 Occurrence Handle1:CAS:528:DC%2BD3cXktFWksL4%3D

    Article  CAS  Google Scholar 

  • C. Nalewajko H. Godmaire (1996) ArticleTitleExtracellular products of Myriophyllum spicatum L. as a function of growth phase and diel cycle Arch. Hydrobiol. 127 345–356

    Google Scholar 

  • R. M. Newman (2004) ArticleTitleBiological control of Eurasian watermilfoil by aquatic insects: Basic insights from an applied problem Arch. Hydrobiol. 159 145–184 Occurrence Handle10.1127/0003-9136/2004/0159-0145

    Article  Google Scholar 

  • R. M. Newman M. E. Borman S. W. Castro (1997) ArticleTitleDevelopmental performance of the weevil Euhrychiopsis lecontei on native and exotic watermilfoil host plants J. North Am. Benthol. Soc. 16 627–634

    Google Scholar 

  • D. M. Oseid J. L. L. Smith (1974) ArticleTitleChronic toxicity of hydrogen sulfide to Gammarus pseudolimnaeus Trans. Am. Fish. Soc. 103 819–822 Occurrence Handle10.1577/1548-8659(1974)103<819:CTOHST>2.0.CO;2 Occurrence Handle1:CAS:528:DyaE2MXhsFShs78%3D

    Article  CAS  Google Scholar 

  • M. L. Ostrofsky E. R. Zettler (1986) ArticleTitleChemical defenses in aquatic plants J. Ecol. 74 279–287 Occurrence Handle1:CAS:528:DyaL28Xit1ajsb8%3D

    CAS  Google Scholar 

  • P. W. Paré J. H. Tumlinson (1999) ArticleTitlePlant volatiles as a defense against insect herbivores Plant Physiol. 121 325–331 Occurrence Handle10517823

    PubMed  Google Scholar 

  • C. R. Roseland M. B. Bates R. B. Carlson C. Y. Oseto (1992) ArticleTitleDiscrimination of sunflower volatiles by the red sunflower seed weevil Entomol. Exp. Appl. 62 99–106 Occurrence Handle10.1007/BF00345480 Occurrence Handle1:CAS:528:DyaK38XisFamu78%3D

    Article  CAS  Google Scholar 

  • J. Rozema J. Staaij Particlevan de L. Olof Bjorn N. Bakker Particlede (1999) Depletion of stratospheric ozone and solar UV-B radiation: Evolution of land plants, UV-screens and functions of polyphenolics J. Rozema (Eds) Stratospheric Ozone Depletion: The Effects of Enhanced UV-B Radiation on Terrestrial Ecosystems Backhuys Publishers Leiden, The Netherlands 1–19

    Google Scholar 

  • J. Ruther T. Meiners J. L. M. Steidle (2002) ArticleTitleRich in phenomena-lacking in terms. A classification of kairomones Chemoecology 12 161–167

    Google Scholar 

  • S. M. Salom J. A. Carlson B. N. Ang D. M. Grosman E. R. Day (1994) ArticleTitleLaboratory evaluation of biologically-based compounds as antifeedants for the Pales weevil, Hylobius pales (Herbst) (Coleoptera: Curculionidae) J. Entomol. Sci. 29 407–419 Occurrence Handle1:CAS:528:DyaK2cXlslejsb4%3D

    CAS  Google Scholar 

  • A. Schmidt Y. H. Su R. Kunze S. Warner M. Hewitt R. D. Slocum U. Ludewig W. B. Frommer M. Desimone (2004) ArticleTitleUPS1 and UPS2 from Arabidopsis mediate high affinity transport of uracil and 5-fluorouracil J. Biol. Chem. 279 44817–44824 Occurrence Handle15308648 Occurrence Handle1:CAS:528:DC%2BD2cXosFymtbs%3D

    PubMed  CAS  Google Scholar 

  • S. P. Sheldon R. P. Creed (1995) ArticleTitleUse of a native insect as a biological control for an introduced weed Ecol. Appl. 5 1122–1132

    Google Scholar 

  • L. E. Smart M. M. Blight A. J. Hick (1997) ArticleTitleEffect of visual cues and a mixture of isothiocyanates on trap capture of cabbage seed weevil, Ceutorhynchus assimilis J. Chem. Ecol. 23 889–902 Occurrence Handle1:CAS:528:DyaK2sXjslCqtbw%3D

    CAS  Google Scholar 

  • C. S. Smith J. W. Barko (1990) ArticleTitleEcology of Eurasian watermilfoil J. Aquat. Plant Manage. 28 55–64

    Google Scholar 

  • S. L. Solarz R. M. Newman (1996) ArticleTitleOviposition specificity and behavior of the watermilfoil specialist Euhrychiopsis lecontei Oecologia 106 337–344 Occurrence Handle10.1007/BF00334561

    Article  Google Scholar 

  • S. L. Solarz R. M. Newman (2001) ArticleTitleVariation in hostplant preference and performance by the milfoil weevil, Euhrychiopsis lecontei Dietz, exposed to native and exotic watermilfoils Oecologia 126 66–75 Occurrence Handle10.1007/s004420000484

    Article  Google Scholar 

  • B. Spänhoff C. Kock A. Meyer E. I. Meyer (2005) ArticleTitleDo grazing caddisfly larvae of Melampophylax mucoreus (Limnephilidae) use their antennae for olfactory food detection? Physiol. Entomol. 30 134–143

    Google Scholar 

  • D. F. Spencer G. G. Ksander (1999) ArticleTitlePhenolic acids and nutrient content for aquatic macrophytes from Fall River, California J. Freshw. Ecol. 14 197–209 Occurrence Handle1:CAS:528:DyaK1MXjvV2ns7k%3D

    CAS  Google Scholar 

  • K. G. Wagner A. I. Backer (1992) ArticleTitleDynamics of nucleotides in plants studied on a cellular basis Int. Rev. Cyt. 134 1–84 Occurrence Handle1:CAS:528:DyaK38XmsVymsrc%3D

    CAS  Google Scholar 

  • O. Walenciak W. Zwisler E. M. Gross (2002) ArticleTitleInfluence of Myriophyllum spicatum-derived tannins on gut microbiota of its herbivore Acentria ephemerella J. Chem. Ecol. 28 2045–2056 Occurrence Handle12474899 Occurrence Handle10.1023/A:1020754012785 Occurrence Handle1:CAS:528:DC%2BD38XnvFOiur0%3D

    Article  PubMed  CAS  Google Scholar 

  • P. G. Waterman (1998) Chemical taxonomy of alkaloids M. F. Roberts M. Wink (Eds) Alkaloids: Biochemistry, Ecology, and Medicinal Applications Plenum Press New York 87–106

    Google Scholar 

  • A. R. Weig C. Jakob (2000) ArticleTitleFunctional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae FEBS Lett. 281 293–298

    Google Scholar 

  • M. J. Weissburg M. C. Ferner D. P. Pisut D. L. Smee (2002) ArticleTitleEcological consequences of chemically mediated prey perception J. Chem. Ecol. 28 1953–1970 Occurrence Handle12474893 Occurrence Handle10.1023/A:1020741710060 Occurrence Handle1:CAS:528:DC%2BD38XnvFOitbk%3D

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Elisabeth M. Gross for the gift of tellimagrandin II and Frank R. Stermitz for analysis of alkaloid content. We are grateful to Tom Krick, Letitia Yao, Beverly Ostrowski, and LeeAnn Higgins for assistance and advice with the mass spectral and NMR analyses. We thank M. Moody for molecular identification of Myriophyllum spp. Assistance with specimen collection and analyses were provided by D. Ward, C. Lemmon, S. Daugherty, S. Coloso, J. Dehn, K. Eichstaedt, C. McCollum, and K. Mann. We thank LeeAnn Higgins and two anonymous reviewers for their comments on the manuscript. This work is sponsored by the Minnesota Sea Grant College Program supported by the NOAA Office of Sea Grant, United States Department of Commerce, under grant no. NOAA-NA16-RG1046. The U.S. government is authorized to reproduce and distribute reprints for government purposes, not withstanding any copyright notation that may appear hereon. Additional support was provided by the Minnesota Agricultural Experiment Station and the University of Minnesota Graduate School. This paper is journal reprint no. JR 511 of the Minnesota Sea Grant College Program.

Author information

Authors and Affiliations

  1. Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, 1980 Folwell Avenue, St. Paul, MN, 55108, USA

    Michelle D. Marko & Raymond M. Newman

  2. Department of Plant Biology, University of Minnesota, 1445 Gortner Avenue, St. Paul, MN, 55108, USA

    Michelle D. Marko & Florence K. Gleason

Authors
  1. Michelle D. Marko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raymond M. Newman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Florence K. Gleason
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florence K. Gleason.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marko, M.D., Newman, R.M. & Gleason, F.K. Chemically Mediated Host-Plant Selection by the Milfoil Weevil: A Freshwater Insect–Plant Interaction. J Chem Ecol 31, 2857–2876 (2005). https://doi.org/10.1007/s10886-005-8399-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-8399-7

Key Words

Search

Navigation