Aquatic Sciences

, Volume 79, Issue 2, pp 309–318 | Cite as

Host plant location by chemotaxis in an aquatic beetle

  • Gregory Röder
  • Matteo Mota
  • Ted C. J. Turlings
Research Article


Interactions between plants and aquatic insects are poorly documented, especially for turbid freshwater ecosystems. Many Swiss lakes offer such habitats, several of which are inhabited by the leaf beetle Macroplea appendiculata (Panzer 1794). This donaciid beetle is the only coleopteran species known to complete its life cycle entirely under water, where it lives primarily on perfoliate pondweed (Potamogeton perfoliatus L.), with Eurasian watermilfoil (Myriophyllum spicatum L.) as an alternative host plant. Direct observations during diving trips, aquatic olfactometer bioassays, and stir bar sorptive extractions (SBSE) coupled with GC–MS analysis were used to understand how these beetles locate their patchily distributed host plants and congeners in a harsh, often swirling environment. In olfactometer assays we observed that the aquatic beetle is strongly attracted to water extracts of pondweed, whereas neither mature males nor females beetles seem to produce attractive cues. The chemical analyses revealed that perfoliate pondweed releases one dominating compound, eucalyptol. Olfactometer assays confirmed that this is a potent attractant for the beetle. We also observed attraction to phytol, which is released by the main, as well as the alternative host plant. These finding are somewhat surprising as eucalyptol has never been reported for aquatic plants and phytol is poorly soluble in water. In addition, both are frequently described as insect repellents in terrestrial ecosystems. We suggest that these terpenoids normally have a defensive function against herbivores and pathogens, but that the highly specialized leaf beetle has evolved to exploit its host’s defence chemistry for optimal foraging.


Aquatic beetle Plant-herbivore interactions Freshwater Macrophytes Host location Macroplea appendicultata Chemical attractants 



We thank Aline Verdon for help with the figures, Aurélien Labhardt for his constructive input, Albert Ros for aquarium material, the Organe d’exécution du service civil ZIVI, the Swiss Biological Records Center, and the Centre national de données et d’informations sur la flore de Suisse for helpful collaboration and information.

Compliance with ethical standards

Conflict of interest

Submission of the manuscript has been approved by all relevant authors and institutions, and all persons entitled to authorship have been so named.


  1. Alzogaray RA, Lucia A, Zerba EN, Masuh HM (2011) Insecticidal activity of essential oils from eleven Eucalyptus spp. and two hybrids: lethal and sublethal effects of their major components on Blattella germanica. J Econ Entomol 104:595–600CrossRefPubMedGoogle Scholar
  2. Babu B, Wu JT (2008) Production of natural butylated hydroxytoluene as an antioxidant by freshwater phytoplankton. J Phycol 44:1447–1454CrossRefPubMedGoogle Scholar
  3. Bernays EA, Chapman RF (1994) Chemicals in plants. In: Bernays EA, Chapman RF (eds) Host-plant selection by phytophagous insects. Chapman & Hall, New York, pp 14–54CrossRefGoogle Scholar
  4. Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181CrossRefGoogle Scholar
  5. Bjostad LB, Hibbard BE (1992) 6-Methoxy-2-benzoxazolinone–a semiochemical for host location by western corn-rootworm larvae. J Chem Ecol 18:931–944CrossRefPubMedGoogle Scholar
  6. Bolser RC, Hay ME, Lindquist N, Fenical W, Wilson D (1998) Chemical defenses of freshwater macrophytes against crayfish herbivory. J Chem Ecol 24:1639–1658CrossRefGoogle Scholar
  7. Brocher F (1912) Recherches sur la respiration des insectes aquatiques adultes–les Haemonia. In: Rousseau E (ed) Annales de biologie lacustre. Bruxelles, p 5–26Google Scholar
  8. Bronmark C, Hansson LA (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109CrossRefGoogle Scholar
  9. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends in Plant Sci 10:269–274CrossRefGoogle Scholar
  10. Carr WES (1988) The molecular nature of chemical stimuli in the aquatic environment. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer-Verlag, New York, pp 3–27CrossRefGoogle Scholar
  11. Chapman RF (2007) Foraging and food choice of phytophagous insect. In: Hardege JD (ed) Chemical ecology. Encyclopedia in life support systems (EOLSS), p 71–101Google Scholar
  12. Cheng L, Roussis V (1998) Sex attractant in the marine insect Trochopus plumbeus (Heteroptera: Veliidae): a preliminary report. Mar Ecol Prog Ser 170:283–286CrossRefGoogle Scholar
  13. Decho AW, Browne KA, Zimmer-Faust RK (1998) Chemical cues: why basic peptides are signal molecules in marine environments. Limnol Oceanogr 43:1410–1417CrossRefGoogle Scholar
  14. Dickens JC (2006) Plant volatiles moderate response to aggregation pheromone in Colorado potato beetle. J Appl Entomol 130:26–31CrossRefGoogle Scholar
  15. Fink P (2007) Ecological functions of volatile organic compounds in aquatic systems. Mar Freshwater Behav Physiol 40:155–168CrossRefGoogle Scholar
  16. Forel FA (1904) In: Cie FR (ed) Le Léman, monographie limnologique, Lausanne, p 715Google Scholar
  17. Glomski LAM, Wood KV, Nicholson RL, Lembi CA (2002) The search for exudates from Eurasian watermilfoil and Hydrilla. J Aquat Plant Manag 40:17–22Google Scholar
  18. Godmaire H, Nalewajko C (1990) Structure and development of secretory trichomes on Myriophyllum spicatum. L Aquat Bot 37:99–121CrossRefGoogle Scholar
  19. Green AJ, Sanchez MI (2006) Passive internal dispersal of insect larvae by migratory birds. Biol Lett 2:55–57CrossRefPubMedGoogle Scholar
  20. Grillas P (1988) Haemonia appendiculata Panzer (Chrysomelidae, Donaciinae) and its impact on Potamogeton pectinatus L and Myriophyllum spicatum L beds in the Camargue (France). Aquat Bot 31:347–353CrossRefGoogle Scholar
  21. Gross EM, Kornijow R (2002) Investigation on competitors and predators of herbivorous aquatic Lepidoptera (Acentria ephemerella) on submersed macrophytes in a large prealpine lake. Verh Internat Verein Limnol 28:721–725Google Scholar
  22. Guerin PM, Städler E, Buser HR (1983) Identification of host plant attractants for the carrot fly, Psila rosae. J Chem Ecol 9:843–861CrossRefPubMedGoogle Scholar
  23. Han BY, Zhang ZN, Fang YL (2001) Electrophysiology and behavior feedback of diamondback moth, Plutella xylostella, to volatile secondary metabolites emitted by Chinese cabbage. Chin Sci Bull 46:2086–2088CrossRefGoogle Scholar
  24. Hiltpold I, Turlings TCJ (2008) Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34:628–635CrossRefPubMedGoogle Scholar
  25. Insam H, Seewald MSA (2010) Volatile organic compounds (VOCs) in soils. Biol Fert Soils 46:199–213CrossRefGoogle Scholar
  26. Kimmerer TW, Kozlowski TT (1982) Ethylene, ethane, acetaldehyde, and ethanol production by plants under stress. Plant Physiol 84:1204–1209CrossRefGoogle Scholar
  27. Kleinschmidt B, Kölsch G (2011) Adopting bacteria in order to adapt to water–how reed beetles colonized the wetlands (Coleoptera, Chrysomelidae, Donaciinae). Insects 2:540–554CrossRefPubMedPubMedCentralGoogle Scholar
  28. Klocke JA, Darlington MV, Balandrin MF (1987) 1,8-Cineole (Eucalyptol), a mosquito feeding and ovipositional repellent from volatile oil of Hemizonia fitchii (Asteraceae). J Chem Ecol 13:2131–2141CrossRefPubMedGoogle Scholar
  29. Kölsch G, Krause A (2011) Oxygen consumption of the aquatic leaf beetles Macroplea mutica and Macroplea appendiculata is low and not influenced by salinity. Physiol Entomol 36:111–119CrossRefGoogle Scholar
  30. Kölsch G, Kubiak M (2011) The aquatic leaf beetle species Macroplea mutica and M. appendiculata (Coleoptera, Chrysomelidae, Donaciinae) differ in their use of Myriophyllum spicatum as host plant. Aquat insects 33:13–26CrossRefGoogle Scholar
  31. Kölsch G, Pedersen BV (2008) Molecular phylogeny of reed beetles (Col, Chrysomelidae, Donaciinae): the signature of ecological specialization and geographical isolation. Mol Phylogenet Evol 48:936–952CrossRefPubMedGoogle Scholar
  32. Kölsch G, Bistrom O, Pedersen BV (2006) Species delimitation in the leaf beetle genus Macroplea (Coleoptera, Chrysomelidae) based on mitochondrial DNA, and phylogeographic considerations. Insect Syst Evol 37:467–479CrossRefGoogle Scholar
  33. Lays P (2006) A fleur d’eau Les donacies. Insectes 140:9–13Google Scholar
  34. Lextrait P, Biemont JC, Pouzat J (1995) Pheromone release by the two forms of Callosobruchus maculatus females: effects of age, temperature and host plant. Physiol Entomol 20:309–317CrossRefGoogle Scholar
  35. Lou Q, Yu P, Liang H (2011) Two new species of Macroplea Samouelle (Coleoptera: Chrysomelidae: Donaciinae) from China, with a key to all known species. Zootaxa 3003:1–21CrossRefGoogle Scholar
  36. Maia MF, Moore SJ (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malar J 10:S11CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mann JS, Crowson RA (1983) Observations on the internal anatomy and classification of Donaciinae (Col, Chrysomelidae). Entomol Month Mag 119:17–27Google Scholar
  38. Marko MD, Newman RM, Gleason FK (2005) Chemically mediated host-plant selection by the milfoil weevil: a freshwater insect-plant interaction. J Chem Ecol 31:2857–2876CrossRefPubMedGoogle Scholar
  39. Medvedev LN (2006) Contributions to the knowledge of the leaf beetles (Coleoptera, Chrysomelidae) of Russia. Entomol Rev 86:457–459CrossRefGoogle Scholar
  40. Mende M, Biström O, Meichssner E, Kölsch G (2010) The aquatic leaf beetle Macroplea mutica (Coleoptera: Chrysomelidae) in Europe: population structure, postglacial colonization and the signature of passive dispersal. Eur J Entomol 107:101–113CrossRefGoogle Scholar
  41. Mohr KH (1985) Beiträge zur Insektenfauna der DDR: Coleoptera–Chrysomelidae: Donaciinae, Orsodacninae, Criocerinae, Clythrinae. Beitr Entomol 35:219–262Google Scholar
  42. Morcia C, Malnati M, Terzi V (2012) In vitro antifungal activity of terpinen-4-ol, eugenol, carvone, 1,8-cineole (eucalyptol) and thymol against mycotoxigenic plant pathogens. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 29:415–422PubMedGoogle Scholar
  43. Ndungu M, Lwande W, Hassanali A, Moreka L, Chander Chhabra S (1995) Cleome monophylla essential oil and its constituents as tick (Rhipicephalus appendiculatus) and maize weevil (Sitophilus zeamais) repellents. Entomol Exp Appl 76:217–222CrossRefGoogle Scholar
  44. Nelson B, Walsh J, Foster G (2007) Finding jewels amongst the reeds: a review of the Irish Donaciine beetles (Coleoptera: Chrysomelidae). Bull Ir Biogeog Soc 31:117–193Google Scholar
  45. Odalo JO, Omolo MO, Malebo H, Angira J, Njeru PM, Ndiege IO, Hassanali A (2005) Repellency of essential oils of some plants from the Kenyan coast against Anopheles gambiae. Acta Trop 95:210–218CrossRefPubMedGoogle Scholar
  46. Ostrofsky ML, Zettler ER (1986) Chemical defenses in aquatic plants. J Ecol 74:279–287CrossRefGoogle Scholar
  47. Otto C (1985) Effects of temporal and spatial variations in food availability on life-cycle and palatability of a chrysomelid beetle (Donacia-Cinerea). Aquat Insects 7:19–28CrossRefGoogle Scholar
  48. Owen JA, Menzies SI (1996) A note on the life history of Macroplea appendicultata (Panzer) (Col: Chrysomelidae). Entomol Rec J Var 108:317–318Google Scholar
  49. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737CrossRefPubMedGoogle Scholar
  50. Reeves JL, Lorch PD (2011) Visual active space of the milfoil weevil, Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae). J Insect Behav 24:264–273CrossRefGoogle Scholar
  51. Reinecke A, Hilker M (2014) Plant semiochemicals–perception and behavioural responses by insects. In: Voelckel C, Jander G (eds), vol 47, chap 4, Annual plant reviews insect-plant interactions, Wiley, UKGoogle Scholar
  52. Robert CAM, Veyrat N, Glauser G, Marti G, Doyen GR, Villard N, Gaillard MDP, Köllner TG, Giron D, Body M, Babst BA, Ferrieri RA, Turlings TCJ, Erb M (2012) A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol Lett 15:55–64CrossRefPubMedGoogle Scholar
  53. Schoonhoven LM, van Loon JJA, Dicke M (2005) In: OUP Oxford (ed), Insect-plant biology 2nd edn. Oxford University, Oxford, p 440Google Scholar
  54. Serandour J, Reynaud S, Willison J, Patouraux J, Gaude T, Ravanel P, Lemperiere G, Raveton M (2008) Ubiquitous water-soluble molecules in aquatic plant exudates determine specific insect attraction. PLoS One 3:e3350CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sfara V, Zerba EN, Alzogaray RA (2009) Fumigant insecticidal activity and repellent effect of five essential oils and seven monoterpenes on first-instar nymphs of Rhodnius prolixus. J Med Entomol 46:511–515CrossRefPubMedGoogle Scholar
  56. Smith CS, Barko JW (1990) Ecology of Eurasian watermilfoil. J Aquat Plant Manag 28:55–64Google Scholar
  57. Solarz SL, Newman RM (1996) Oviposition specificity and behavior of the watermilfoil specialist Euhrychiopsis lecontei. Oecologia 106:337–344CrossRefGoogle Scholar
  58. Städler E (1992) Behavioral responses of insects to plant secondary compounds. In: Rosenthal GA, Berenbaum MR (eds.) Herbivores–their interactions with secondary plant metabolites 2nd edn. Academic Press Inc, San Diego, vol 2, p 45–79Google Scholar
  59. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna. http://www.R-projectorg
  60. Turlings TCJ, Davison AC, Tamò C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomo 29:44–55CrossRefGoogle Scholar
  61. Weissburg MJ, Ferner MC, Pisut DP, Smee DL (2002) Ecological consequences of chemically mediated prey perception. J Chem Ecol 28:1953–1970CrossRefPubMedGoogle Scholar
  62. Wetzel RG (2001) Bacterioplankton & Detritus: organic carbon cycling and ecosystem metabolism. In: Limnology: lake and river ecosystems. Academic Press, London, p 489–525 (731–783) Google Scholar
  63. Zengin H, Baysal AH (2014) Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 19:17773–17798CrossRefPubMedGoogle Scholar
  64. Zhang J, Wheeler GS, Purcell M, Ding J (2010) Biology, distribution, and field host plants of Macroplea japana in China: an unsuitable candidate for biological control of Hydrilla verticillata. Fla Entomol 93:116–119CrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  • Gregory Röder
    • 1
  • Matteo Mota
    • 2
  • Ted C. J. Turlings
    • 1
  1. 1.FARCE Laboratory, Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland
  2. 2.Ecole d’Ingénieurs de Changins (HES-SO), Sciences de la TerreNyonSwitzerland

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