, Volume 179, Issue 4, pp 1147–1158 | Cite as

Costs and benefits of plant allelochemicals in herbivore diet in a multi enemy world

  • J. H. Reudler
  • C. Lindstedt
  • H. Pakkanen
  • I. Lehtinen
  • J. Mappes
Plant-microbe-animal interactions - Original research


Sequestration of plant defensive chemicals by herbivorous insects is a way of defending themselves against their natural enemies. Such herbivores have repeatedly evolved bright colours to advertise their unpalatability to predators, i.e. they are aposematic. This often comes with a cost. In this study, we examined the costs and benefits of sequestration of iridoid glycosides (IGs) by the generalist aposematic herbivore, the wood tiger moth, Parasemia plantaginis. We also asked whether the defence against one enemy (a predator) is also effective against another (a parasitoid). We found that the larvae excrete most of the IGs and only small amounts are found in the larvae. Nevertheless, the amounts present in the larvae are sufficient to deter ant predators and also play a role in defence against parasitoids. However, excreting and handling these defensive plant compounds is costly, leading to longer development time and lower pupal mass. Interestingly, the warning signal efficiency and the amount of IGs in the larvae of P. plantaginis are negatively correlated; larvae with less efficient warning signals contain higher levels of chemical defence compounds. Our results may imply that there is a trade-off between production and maintenance of coloration and chemical defence. Although feeding on a diet containing IGs can have life-history costs, it offers multiple benefits in the defence against predators and parasitoids.


Bio assay Cotesia villana Iridoid glycosides Plantago lanceolata Warning signal 



We would like to thank Kaisa Suisto for rearing the P. plantaginis larvae used in the experiments and Emily Burdfield-Steel and an anonymous reviewer for very helpful comments on previous versions of the manuscript. Further, we thank Nåtö Biological Station for providing accommodation during the field work. This research was funded by the Centre of Excellence in Biological Interactions and Academy of Finland Grant #SA-128528 and 218372.

Author contribution statement

JHR originally formulated the idea, JHR, CL and JM developed methodology, JHR and IL conducted field and laboratory work, HP developed methods for chemical analyses, JHR performed statistical analyses, and JHR, CL and JM wrote the manuscript.


  1. Abbott J (2014) Self-medication in insects: current evidence and future perspectives. Ecol Entomol 39:273–280CrossRefGoogle Scholar
  2. Barbosa P, Saunders JA, Kemper J, Trumbule R, Olechno J, Martinat P (1986) Plant allelochemicals and insect parasitoids. Effects of nicotine on Cotesia congregata (Say) (Hymenoptera, Braconidae) and Hyposoter annulipes (Cresson) (Hymenoptera, Ichneumonidae). J Chem Ecol 12:1319–1328CrossRefPubMedGoogle Scholar
  3. Barton KE (2007) Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. Am J Bot 94:56–66CrossRefPubMedGoogle Scholar
  4. Bellman H (2007) Vlinders, rupsen en waardplanten. Tirion, BaarnGoogle Scholar
  5. Berenbaum M, Zangerl AR (1993) Furanocoumarin metabolism in Papilio polyxenes: biochemistry, genetic variability, and ecological significance. Oecologia 95:370–375CrossRefGoogle Scholar
  6. Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B 276:871–877CrossRefGoogle Scholar
  7. Bowers MD (1988) Chemistry and coevolution: Iridoid glycosides, plants and herbivorous insects. In: Spencer K (ed) Chemical Mediation of Coevolution. Academic, New York, pp 133–165CrossRefGoogle Scholar
  8. Bowers MD (1991) Iridoid glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic, San Diego, pp 297–325CrossRefGoogle Scholar
  9. Bowers MD (1992) Unpalatability and the cost of chemical defense in insects. In: Roitberg BD, Isman MB (eds) Chemical ecology of insects: an evolutionary approach. Chapman and Hall, New York, pp 216–244Google Scholar
  10. Bowers MD (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, New York, pp 331–371Google Scholar
  11. Bowers MD, Collinge SK (1992) Fate of iridoid glycosides in different life stages of the buckeye, Junonia coenia (Lepidoptera, Nymphalidae). J Chem Ecol 18:817–831CrossRefPubMedGoogle Scholar
  12. Bowers MD, Collinge SK, Gamble SE, Schmitt J (1992) Effects of genotype, habitat, and seasonal-variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201–207CrossRefGoogle Scholar
  13. Bowers MD, Stamp NE (1992) Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J Chem Ecol 18:985–995CrossRefPubMedGoogle Scholar
  14. Bowers MD, Stamp NE (1993) Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791CrossRefGoogle Scholar
  15. Bowers MD, Stamp NE (1997) Fate of host-plant iridoid glycosides in lepidopteran larvae of Nymphalidae and Arctiidae. J Chem Ecol 23:2955–2965CrossRefGoogle Scholar
  16. Brattsten LB (1988) Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. J Chem Ecol 5:1919–1939CrossRefGoogle Scholar
  17. Camara MD (1997) Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable? J Chem Ecol 23:2093–2106CrossRefGoogle Scholar
  18. Cornell HV, Hawkins BA (1995) Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am Nat 145:563–593CrossRefGoogle Scholar
  19. Cornell HV, Hawkins BA, Hochberg ME (1998) Towards an empirically-based theory of herbivore demography. Ecol Entomol 23:340–349CrossRefGoogle Scholar
  20. Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: consipicuouness versus toxicity in poison frogs. Proc Natl Acad Sci USA 103:5852–5857CrossRefPubMedCentralPubMedGoogle Scholar
  21. Dempster JP (1983) The natural control of populations of butterflies and moths. Biol Rev 58:461–481CrossRefGoogle Scholar
  22. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307CrossRefPubMedGoogle Scholar
  23. Duff RB, Bacon JSD, Mundie CM, Farmer VC, Russell JD, Forrester AR (1965) Catalpol and methylcatalpol: naturally ocurring glycosides in Plantago and Buddleia species. Biochem J 96:1–5CrossRefPubMedCentralPubMedGoogle Scholar
  24. Duffey SS (1980) Sequestration of plant natural products by insects. Annu Rev Entomol 25:447–477CrossRefGoogle Scholar
  25. Dyer LA (1995) Tasty generalists and nasty specialists? Antipredator mechanisms in tropical lepidopteran larvae. Ecology 76:1483–1496CrossRefGoogle Scholar
  26. Dyer LA (1997) Effectiveness of caterpillar defenses against three species of invertebrate predators. J Res Lepid 34:48–68Google Scholar
  27. Dyer LA, Bowers MD (1996) The importance of sequestered iridoid glycosides as a defense against an ant predator. J Chem Ecol 22:1527–1539CrossRefPubMedGoogle Scholar
  28. Dyer LA, Dodson CD, Gentry G (2003a) A bioassy for insect deterrent compounds found in plant and animal tissues. Phytochem Anal 14:381–388CrossRefPubMedGoogle Scholar
  29. Dyer LA et al (2003b) Synergistic effects of three Piper amides on generalist and specialist herbivores. J Chem Ecol 29:2499–2514CrossRefPubMedGoogle Scholar
  30. English-Loeb GM, Brody AK, Karban R (1993) Host-plant-mediated interactions between a generalist folivore and its tachinid parasitoid. J Anim Ecol 63:465–471CrossRefGoogle Scholar
  31. Friman V-P, Lindstedt C, Hiltunen T, Laakso J, Mappes J (2009) Predation on multiple trophic levels shapes the evolution of pathogen virulence. PLoS ONE 4:e6761CrossRefPubMedCentralPubMedGoogle Scholar
  32. Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741CrossRefPubMedGoogle Scholar
  33. Gauld ID, Gaston KJ (1994) The taste of enemy-free space: parasitoids and nasty hosts. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, New York, pp 279–299Google Scholar
  34. Gentry G, Dyer LA (2002) On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119CrossRefGoogle Scholar
  35. Guilford T, Dawkins MS (1993) Are warning colors handicaps? Evolution 47:400–416CrossRefGoogle Scholar
  36. Gunasena GH, Vinson SB, Williams HJ (1990) Effects of nicotine on growth, development, and survival of the tobacco budworm (Lepidoptera, Noctuidae) and the parasitoid Campoletis sonorensis (Hymenoptera, Ichneumonidae). J Econ Entomol 83:1777–1782CrossRefGoogle Scholar
  37. Hare JF, Eisner T (1993) Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatix eggs-effects of alkaloid concentration, oxidation-state, and prior exposure of ants to alkaloid-laden prey. Oecologia 96:9–18CrossRefGoogle Scholar
  38. Higginson AD, Delf J, Ruxton GD, Speed MP (2011) Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae. J Anim Ecol 80:384–392CrossRefPubMedGoogle Scholar
  39. Honek A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–792CrossRefGoogle Scholar
  40. Johnson KS (1999) Comparative detoxification of plant (Magnolia virginiana) allelochemicals by generalist and specialist Saturniid silkmoths. J Chem Ecol 25:253–269CrossRefGoogle Scholar
  41. Jones CG, Whitman DW, Compton SJ, Silk PJ, Blum MS (1989) Reduction in diet breadth results in sequestration of plant chemicals and increases efficacy of chemical defense in a generalist grasshopper. J Chem Ecol 15:1811–1822CrossRefPubMedGoogle Scholar
  42. Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280CrossRefPubMedGoogle Scholar
  43. Lampert EC, Bowers MD (2010) Host plant influences on iridoid glycoside sequestration of generalist and specialist caterpillars. J Chem Ecol 36:1101–1104CrossRefPubMedGoogle Scholar
  44. Lanza J (1988) Ant preferences for passiflora nectar mimics that contain amino acids. Biotropica 20:341–344CrossRefGoogle Scholar
  45. Lee TJ, Marples NM, Speed MP (2010) Can dietary conservatism explain the primary evolution of aposematism? Anim Behav 79:63–74CrossRefGoogle Scholar
  46. Leimar O, Enquist M, Sillén-Tullberg B (1986) Evolutionary stability of aposematic colorarion and prey unprogitability: a theoratical analysis. Am Nat 128:469–490CrossRefGoogle Scholar
  47. Leraut P (ed) (2006) Moths of Europe Volume 1: Saturnids, Lasiocampids, Hawkmoths, Tiger Moths. NAP Editions, Verrieres le BuissonGoogle Scholar
  48. Lindstedt C (2008) Maintenance of variationin warning signals under opposing selection pressures. PhD thesis, University of Jyväskylä, JyväskyläGoogle Scholar
  49. Lindstedt C, Lindstrom L, Mappes J (2008) Hairiness and warning colours as components of antipredator defence: additive or interactive benfits? Anim Behav 75:1703–1713CrossRefGoogle Scholar
  50. Lindstedt C, Lindström L, Mappes J (2009) Thermoregulation can constrain effective warning signal expression. Evolution 63:469–478CrossRefPubMedGoogle Scholar
  51. Lindstedt C, Reudler Talsma JH, Ihalainen E, Lindstrom L, Mappes J (2010) Diet quality affects warning coloration indirectly: excretion costs in a generalist herbivore. Evolution 64:68–78CrossRefPubMedGoogle Scholar
  52. Marak HB, Biere A, van Damme JMM (2000) Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J Evol Biol 13:985–996CrossRefGoogle Scholar
  53. Marttila O, Saarinen K, Haahtela T, Pajari M (1996) Suomen kiitäjät ja kehrääjät. Kirjayhtymä, PorvooGoogle Scholar
  54. Mason PA, Singer MS (2015) Defensive mixology: combining acquired chemicals towards defence. Funct Ecol 29:441–450CrossRefGoogle Scholar
  55. Molleman F, Kaasik A, Whitaker MR, Carey JR (2012) Partitioning variation in duration of ant feeding bouts can offer insights into the palatability of insects: experiments of African fruit-feeding butterflies. J Res Lepid 45:65–75Google Scholar
  56. Nieminen M, Suomi J, van Nouhuys S, Sauri P, Riekkola ML (2003) Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J Chem Ecol 29:823–844CrossRefPubMedGoogle Scholar
  57. Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92CrossRefPubMedGoogle Scholar
  58. Nokelainen O, Valkonen J, Lindstedt C, Mappes J (2012) Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths. J Anim Ecol 83:598–605CrossRefGoogle Scholar
  59. Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivores and natural enemy interactions. Annu Rev Entomol 51:161–185CrossRefGoogle Scholar
  60. Ojala K, Julkunen-Titto R, Lindstrom L, Mappes J (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170Google Scholar
  61. Ojala K, Lindstrom L, Mappes J (2007) Life-history constraints and warning signal expression in an arctiid moth. Funct Ecol 21:1162–1167CrossRefGoogle Scholar
  62. Opitz SEW, Jensen SR, Müller C (2010) Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defense against ants. J Chem Ecol 36:148–157CrossRefPubMedGoogle Scholar
  63. Pabis K (2007) New species of Lepidoptera for the Biogradska Gora National Park, Montenegra. Glas Republ Zavoda Zas Prirode Podgor 29–30:167–169Google Scholar
  64. Poitout S, Bues R (1974) Élevage de chenilles de vingt-huit espèces de Lépidoptères Noctuidae at de deux espèces d’Arctiidae sur milieu artificiel simple. Particularites de L’élevage selon les espèces. Ann Zool Ecol Anim 6:431–441Google Scholar
  65. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  66. Reudler Talsma JH, Tori K, van Nouhuys S (2008) Host plant use by the Heath fritillary butterfly, Melitaea athalia: plant habitat, species and chemistry. Arthropod-Plant Interactions 2:63–75CrossRefGoogle Scholar
  67. Richards LA, Dyer LA, Smilanich AM, Dodson CD (2010) Synergistic effects of amides from two piper species on generalist and specialist herbivores. J Chem Ecol 36:1105–1113CrossRefPubMedGoogle Scholar
  68. Rimpler H (1991) Sequestration of iridoids by insects. In: Harbone JB, Thomas Barberan FA (eds) Ecological Chemistry and Biochemistry of Plant Terpenoids. Clarendon Press, OxfordGoogle Scholar
  69. Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernández LM (2010) HOSTS—a Database of the World’s Lepidopteran Hostplants, vol 2010. Natural History Museum, LondonGoogle Scholar
  70. Rothschild M (1985) British aposematic lepidoptera. In: Heath J, Emmet AM (eds) The moths and butterflies of Great Britain and Ireland. Harley Books, Essex, pp 9–62Google Scholar
  71. Rothschild M, Aplin RT, Cockrum PA, Edgar JA, Fairweather P, Lees R (1979) Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of the secondary plant substances in the Arctiidae. Biol J Linn Soc 12:305–326CrossRefGoogle Scholar
  72. Sagar GR, Harper JL (1964) Biological flora of the British isles. Plantago major L., Plantago media L. and Plantago lanceolata L. J Ecol 52:189–221CrossRefGoogle Scholar
  73. Sherratt TN (2002) The coevolution of warning signals. Proc R Soc Lond B 269:741–746CrossRefGoogle Scholar
  74. Singer MS, Lichter-Marck IH, Farkas TE, Aaron E, Whitney KD, Mooney KA (2014) Herbivore diet breadth mediates the cascading effects of carnivores in food webs. Proc Natl Acad Sci USA 111:9521–9526CrossRefPubMedCentralPubMedGoogle Scholar
  75. Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONEne 4:e4796CrossRefPubMedCentralPubMedGoogle Scholar
  76. Singer MS, Rodrigues D, Stireman JO, Carrière Y (2004) Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology 85:2747–2753Google Scholar
  77. Smilanich AM, Dyer LA, Chambers JQ, Bowers MD (2009) Immunological cost of chemical defence and the evolution of herbivore diet breath. Ecol Lett 12:612–621CrossRefPubMedGoogle Scholar
  78. Speed MP, Ruxton GD (2005) Warning displays in spiny animals: one (more) evolutionary route to aposematism. Evolution 59:2499–2508CrossRefPubMedGoogle Scholar
  79. Speed MP, Ruxton GD, Mappes J, Sherratt T (2013) Why are defensive toxins so variable? An evolutionary perpective. Biol Rev 87:874–884CrossRefGoogle Scholar
  80. Stephenson AG (1981) Toxic nectar deters nectar thieves of Catalpa speciosa. Am Midl Nat 105:381–383CrossRefGoogle Scholar
  81. Stermitz FR, Kader MSA, Foderaro TA, Pomeroy M (1994) Iridoid glycosides from some butterflies and their larval food plants. Phytochemistry 37:997–999CrossRefGoogle Scholar
  82. Suomi J, Sirén H, Jussila M, Wiedner SK, Riekkola ML (2003) Determination of iridoid glycosides in larvae and adults of butterfly Melitaea cinxia by partial filling micellar electrokinetic capillary chromatography-electrospray ionisation mass spectrometry. Anal Bioanal Chem 376:884–889CrossRefPubMedGoogle Scholar
  83. Weller SJ, Jacobsen NL, Conner WE (1999) The evolution of chemical defences and mating systems in tiger moths (Lepidoptera: Arctiidae). Biol J Linn Soc 68:557–578CrossRefGoogle Scholar
  84. Willinger G, Dobler S (2001) Selective sequestration of iridoid glycosides from their host plants in Longitarsus flea beetles. Biochem Syst Ecol 29:335–346CrossRefPubMedGoogle Scholar
  85. Von Nickisch-Rosenegk E, Wink M (1993) Sequestration of pyrrolizdine alkaloids in several arctiid moths (Lepidoptera: Arctiidae). J Chem Ecol 19:1889–1903CrossRefGoogle Scholar
  86. Zhang J, Friman V-P, Laakso J, Mappes J (2012) Interactive effects between diet and genotypes of host and pathogen define the severity of infection. Ecol Evol 2:2347–2356CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • J. H. Reudler
    • 1
  • C. Lindstedt
    • 1
  • H. Pakkanen
    • 2
  • I. Lehtinen
    • 1
    • 3
  • J. Mappes
    • 1
  1. 1.Department of Biology and Environmental Science, Centre of Excellence in Biological InteractionsUniversity of JyvaskylaJyväskyläFinland
  2. 2.Department of Chemistry, Laboratory of Applied ChemistryUniversity of JyvaskylaJyväskyläFinland
  3. 3.Department of Environmental SciencesUniversity of HelsinkiHelsinkiFinland

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