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Effects of pyrrolizidine alkaloids through different trophic levels

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Abstract

Pyrrolizidine alkaloids (PAs), mainly those with a 1,2-double bond in the necine base moiety (=1,2-dehydropyrrolizidines), constitute a class of well studied compounds with respect to their flux through different trophic levels. Plants belonging to various clades (e.g. Echiteae, Eupatorieae and Senecioneae, Boraginaceae, and Crotalarieae) biosynthesize PAs as N-oxides, generally in the roots, and transport them through the phloem to stems, leaves, and reproductive structures, where they act as potent deterrents against non-specialist herbivores. On the other hand, PA specialist herbivores (mainly arctiid moths, danaine and ithomiine butterflies, and some leaf beetles) have become able to overcome this chemical barrier, and to sequester these alkaloids from their larval host plants or from sources visited by adults, such as flowers and dead or withered plants. Specialists use PAs for their own benefit as chemical defence against a vast array of predators (e.g. ants, lacewings, spiders, lizards, birds, and mammals), but some predators are able to feed on PA-insects, by avoiding or physiologically overcoming PAs present in tissues of the ingested prey. Parasitoids may be affected by PAs, depending on their degree of specialization in relation to PA-insects. Arctiidae, Danainae and Ithomiinae also use PAs as precursors of sexual pheromones. The effects of PAs on trophic interactions have been intensely studied over the last four decades, but some open questions remain, and are discussed, such as the underlying mechanisms that lead to PA diversification, activity of different PA structures, synergism among PAs and other so-called defensive substances in PA-plants, and the ability to overcome this chemical barrier by predators and parasitoids.

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References

  • Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420

    Google Scholar 

  • Agrawal AA, Salminen J-P, Fishbein M (2009) Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution 63:663–673

    PubMed  CAS  Google Scholar 

  • Aplin RT, Benn MH, Rothschild M (1968) Poisonous alkaloids in the body tissues of the cinnabar moth (Callimorpha jacobaeae). Nature 219:747–748

    CAS  Google Scholar 

  • Bates HW (1862) Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae. Trans Linn Soc Lond 23:495–566

    Google Scholar 

  • Belt T (1888) The Naturalist in Nicaragua, 2nd edn. Edward Bumpus, London (reprinted by University of Chicago Press, 1985)

    Google Scholar 

  • Benn M, Degrave J, Gnanasunderam C, Hutchins R (1979) Host-plant pyrrolizidine alkaloids in Nyctemera annulata Boisduval: their persistence through the lifecycle and transfer to a parasite. Experientia 35:731–732

    CAS  Google Scholar 

  • Bentley MD, Leonard DE, Stoddard WF, Zalkow LH (1984) Pyrrolizidine alkaloids as larval feeding deterrents for spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Ann Entomol Soc Am 77:393–397

    CAS  Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman & Hall, New York

    Google Scholar 

  • Bernays EA, Edgar JA, Rothschild M (1977) Pyrrolizidine alkaloids sequestered and stored by the aposematic grasshopper Zonocerus variegatus. J Zool 182:85–87

    Google Scholar 

  • Bezzerides A, Yong TH, Bezzerides J, Husseini J, Ladau J, Eisner M, Eisner T (2004) Plant-derived pyrrolizidine alkaloid protects eggs of a moth (Utetheisa ornatrix) against a parasitoid wasp (Trichogramma ostriniae). Proc Natl Acad Sci USA 101:9029–9032

    PubMed  CAS  Google Scholar 

  • Biller A, Boppré M, Witte L, Hartmann T (1994) Pyrrolizidine alkaloids in Chromolaena odorata: chemical and chemoecological aspects. Phytochemistry 35:615–619

    CAS  Google Scholar 

  • Boppré M (1981) Adult Lepidoptera “feeding” at withered Heliotropium plants (Boraginaceae) in East Africa. Ecol Entomol 6:449–452

    Google Scholar 

  • Boppré M (1983) Leaf-scratching—a specialized behaviour of danaine butterflies (Lepidoptera) for gathering secondary plant substances. Oecologia 59:414–416

    Google Scholar 

  • Boppré M (1984a) Redefining “pharmacophagy”. J Chem Ecol 10:1151–1154

    Google Scholar 

  • Boppré M (1984b) Chemically mediated interactions between butterflies. In: Vane-Wright RI, Ackery PR (eds) The Biology of Butterflies. Princeton University Press, Princeton

    Google Scholar 

  • Boppré M (1986) Insects pharmacophagously utilizing defensive plant-chemicals (pyrrolizidine alkaloids). Naturwissenschaften 73:17–26

    Google Scholar 

  • Boppré M (1990) Lepidoptera and pyrrolizidine alkaloids. Exemplification of complexity in chemical ecology. J Chem Ecol 16:165–185

    Google Scholar 

  • Boppré M (1999) ‘Drug-addicted’ insects in Africa. Metamorphosis 10:3–15

    Google Scholar 

  • Brehm G, Hartmann T, Willmott K (2007) Pyrrolizidine alkaloids and pharmacophagous Lepidoptera visitors of Prestonia amabilis (Apocynaceae) in a montane rainforest in Ecuador. Ann Missouri Bot Gard 94:463–473

    Google Scholar 

  • Brower LP, Brower JVZ (1964) Birds, butterflies, and plant poisons: a study in ecological chemistry. Zoologica 49:137–159

    CAS  Google Scholar 

  • Brown KS (1984) Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator. Nature 309:707–709

    CAS  Google Scholar 

  • Brown KS (1985) Chemical ecology of dehydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae). Rev Bras Biol 44:435–460

    Google Scholar 

  • Brown KS, Trigo JR (1995) The ecological activity of alkaloids. In: Cordell GA (ed) The alkaloids, vol 47. Academic Press, New York, pp 227–354

    Google Scholar 

  • Brown KS, Vasconcellos-Neto J (1976) Predation on aposematic ithomiine butterflies by tanagers (Pipraeidea melanonota). Biotropica 8:136–141

    Google Scholar 

  • Cardoso MZ (1997) Testing chemical defense based on pyrrolizidine alkaloids. Animal Behav 54:985–991

    Google Scholar 

  • Chai P (1986) Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol J Linn Soc 29:161–189

    Google Scholar 

  • Cheng D, Klinkhamer PGL (2010) The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of pyrrilizodine alkaloid in Senecio species. Phytochem Rev (in press)

  • Conner WE (2009) Utetheisa ornatrix, the ornate arctiid. In: Conner WE (ed) Tiger moths and woolly bears. Behaviour,ecology, and evolution of the Arctiidae. Oxford University Press, New York

    Google Scholar 

  • Conner WE, Jordan AT (2009) From armaments to ornaments: the relationship between chemical defense and sex in tiger moths. In: Conner WE (ed) Tiger moths and woolly bears. Behaviour, ecology, and evolution of the Arctiidae. Oxford University Press, New York

    Google Scholar 

  • Conner WE, Weller SJ (2004) A quest for alkaloids: the curious relationship of tiger moths and plants containing pyrrolizidine alkaloids. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Campbridge University Press, New York

    Google Scholar 

  • Conner WE, Eisner T, Vandermeer RK, Guerrero A, Meinwald J (1981) Pre-copulatory sexual interaction in an arctiid moth (Utetheisa ornatrix)—role of a pheromone derived from dietary alkaloids. Behav Ecol Sociobiol 9:227–235

    Google Scholar 

  • Culvenor CCJ, Edgar JA, Jago MV, Outteridge A, Peterson JE, Smith LW (1976) Hepato- and pneumotoxicity of pyrrolizidine alkaloids and derivatives in relation to molecular structure. Chem Biol Interact 12:299–324

    PubMed  CAS  Google Scholar 

  • Del Campo ML, Possner ST, Eisner T (2007) Corematal function in Utetheisa ornatrix (Lepidoptera: Arctiidae): hydroxydanaidal is devoid of intrinsic defensive potency. Chemoecology 17:19–22

    CAS  Google Scholar 

  • Dias AT, Trigo JR, Lewinsohn TM (2010) Bottom-up effects on a plant-endophage-parasitoid system: the role of flower-head size and chemistry. Austral Ecol 35:104–115

    Google Scholar 

  • Dreyer DL, Jones KC, Molyneux RJ (1985) Feeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrthosiphon pisum) and evidence for phloem transport of indolizidine alkaloid swainsonine. J Chem Ecol 11:1045–1051

    CAS  Google Scholar 

  • Dussourd DE, Ubik K, Harvis C, Resch J, Meinwald J, Eisner T (1988) Biparental defensive endowment of eggs with acquired plant alkaloid in the moth Utetheisa ornatrix. Proc Natl Acad Sci USA 85:5992–5996

    PubMed  CAS  Google Scholar 

  • Dussourd DE, Harvis CA, Resch J, Meinwald J, Eisner T (1991) Pheromonal advertisement of a nuptial gift by a male moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 88:9224–9227

    PubMed  CAS  Google Scholar 

  • Edgar JA (1975) Danainae (Lep.) and 1,2-dehydropyrrolizidine alkaloid-containing plants–with reference to observations made in New Hebrides. Phil Trans R Soc Lond B 272:467–476

    Google Scholar 

  • Egelhaaf A, Cölln K, Schmitz B, Buck M, Wink M, Schneider D (1990) Organ specific storage of dietary pyrrolizidine alkaloids in the arctiid moth Creatonotos transiens. Z Naturforsch 45c:115–120

    Google Scholar 

  • Eisner T (1982) For love of nature: exploration and discovery at biological field stations. Bioscience 32:321–326

    CAS  Google Scholar 

  • Eisner T, Eisner M (1991) Unpalatability of the pyrrolizidine alkaloid-containing moth Utetheisa ornatrix, and its larva, to wolf spiders. Psyche 98:111–118

    Google Scholar 

  • Eisner T, Meinwald J (1995) The chemistry of sexual selection. Proc Natl Acad Sci USA 92:50–55

    PubMed  CAS  Google Scholar 

  • Eisner T, Eisner M, Rossini C, Iyengar VK, Roach BL, Benedikt E, Meinwald J (2000) Chemical defense against predation in an insect egg. Proc Natl Acad Sci USA 97:1634–1639

    PubMed  CAS  Google Scholar 

  • Ferro VG, Guimarães PR, Trigo JR (2006) Why do larvae of Utetheisa ornatrix penetrate and feed in pods of Crotalaria species? Larval performance vs. chemical and physical constraints. Entomol Exp Appl 121:23–29

    Google Scholar 

  • Flores AS, Tozzi AMGA, Trigo JR (2009) Pyrrolizidine alkaloid profiles in Crotalaria species from Brazil: chemotaxonomic significance. Biochem Syst Ecol 37:459–469

    CAS  Google Scholar 

  • Frölich C, Hartmann T, Ober D (2006) Tissue distribution and biosynthesis of 1,2-saturated pyrrolizidine alkaloids in Phalaenopsis hybrids (Orchidaceae). Phytochemistry 67:1493–1502

    PubMed  Google Scholar 

  • Futuyma DJ, Keese MC (1992) Evolution and coevolution of plants and phytophagous arthropods. In: Rosenthal GA, Berenbaum MR (eds) Herbivores. Their interactions with secondary plant metabolites, vol II, 2nd edn. Academic Press, New York

    Google Scholar 

  • Gassmann AJ, Stock SP, Tabashnik BE, Singer MS (2010) Tritrophic effects of host plants on an herbivore-pathogen interaction. Ann Entomol Soc Am 103:371–378

    Google Scholar 

  • Glendinning JI, Brower LP, Montgomery CA (1990) Responses of three mouse species to deterrent chemicals in monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline. Chemoecology 1:114–123

    CAS  Google Scholar 

  • Hägele B, Rowell-Rahier M (2000) Choice, performance and heritability of performance of specialist and generalist insect herbivores towards cacalol and seneciphylline, two allelochemicals of Adenostyles alpina (Asteraceae). J Evol Biol 13:131–142

    Google Scholar 

  • Harber WA (1978) Evolutionary ecology of tropical mimetic butterflies (Lepidoptera: Ithomiiae). PhD thesis, University of Minnesota

  • Hare J, Eisner T (1993) Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs: effect of alkaloid concentration, oxidation state, and prior exposure of ants to alkaloid-laden prey. Oecologia 96:9–18

    Google Scholar 

  • Hartmann T (2009) Pyrrolizidine alkaloids: the successful adoption of a plant chemical defense. In: Conner WE (ed) Tiger moths and woolly bears. Behaviour, ecology, and evolution of the Arctiidae. Oxford University Press, New York

    Google Scholar 

  • Hartmann T, Ober D (2008) Defense by pyrrolizidine alkaloids: developed by plants and recruited by insects. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York

    Google Scholar 

  • Hartmann T, Witte L (1995) Chemistry, biology and chemoecology of the pyrrolizidine alkaloids. In: Pelletier SW (ed) Alkaloids. Chemical and biological perspectives, vol 9. Pergamon Press, Oxford, pp 155–233

    Google Scholar 

  • Hartmann T, Häggström H, Theuring C, Lindigkeit R, Rahier M (2003) Detoxification of pyrrolizidine alkaloids by the harvestman Mitopus morio (Phalangidae) a predator of alkaloid defended leaf beetles. Chemoecology 13:123–127

    CAS  Google Scholar 

  • Hartmann T, Theuring C, Beuerle T, Klewer N, Schulz S, Singer MS, Bernays EA (2005a) Specific recognition, detoxification and metabolism of pyrrolizidine alkaloids by the polyphagous arctiid Estigmene acrea. Insect Biochem Mol Biol 35:391–411

    PubMed  CAS  Google Scholar 

  • Hartmann T, Theuring C, Beuerle T, Bernays EA, Singer MS (2005b) Acquisition, transformation and maintenance of plant pyrrolizidine alkaloids by the polyphagous arctiid Grammia geneura. Insect Biochem Mol Biol 35:1083–1099

    PubMed  CAS  Google Scholar 

  • Hol WHG, Van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772

    PubMed  CAS  Google Scholar 

  • Honda K, Hayashi N, Abe F et al (1997) Pyrrolizidine alkaloids mediate host-plant recognition by ovipositing females of an old world danaid butterfly, Idea leuconoe. J Chem Ecol 23:1703–1713

    CAS  Google Scholar 

  • Hristov N, Conner WE (2005a) Effectiveness of tiger moth (Lepidoptera, Arctiidae) chemical defenses against an insectivorous bat (Eptesicus fuscus). Chemoecology 15:105–113

    Google Scholar 

  • Hristov NI, Conner WE (2005b) Sound strategy: acoustic aposematism in the bat-tiger moth arms race. Naturwissenschaften 92:164–169

    PubMed  CAS  Google Scholar 

  • Iyengar VK, Rossini C, Hoebeke ER, Conner WE, Eisner T (1999) First record of the parasitoid Archytas aterrimus (Diptera: Tachinidae) from Utetheisa ornatrix (Lepidoptera: Arctiidae). Entomol News 110:144–146

    Google Scholar 

  • Jenett-Siems K, Ott SC, Schimming T, Siems K, Muller F, Hilker M, Witte L, Hartmann T, Austin DF, Eich E (2005) Ipangulines and minalobines, chemotaxonomic markers of the infrageneric Ipomoea taxon subgenus Quamoclit, section Mina. Phytochemistry 66:223–231

    PubMed  CAS  Google Scholar 

  • Jordan AT, Jones TH, Conner WE (2007) Morphogenetic effects of alkaloidal metabolites on the development of the coremata in the salt marsh moth, Estigmene acrea (Dru.) (Lepidoptera: Arctiidae). Arch Insect Biochem Physiol 66:183–189

    PubMed  CAS  Google Scholar 

  • Kirk H, Vrieling K, Van Der Meijden E, Klinkhamer PGL (2010) Species by environment interactions affect pyrrolizidine alkaloid expression in Senecio jacobaea, Senecio aquaticus, and their hybrids. J Chem Ecol 36:378–387

    PubMed  CAS  Google Scholar 

  • Klitzke CF, Trigo JR (2000) New records of pyrrolizidine alkaloid feeding insects. Hemiptera and Coleoptera on Senecio brasiliensis. Biochem Syst Ecol 28:313–318

    PubMed  CAS  Google Scholar 

  • Kowalchuk GA, Hol WHG, Van Veen JA (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38:2852–2859

    CAS  Google Scholar 

  • Landolt PJ, Lenczewski B (1993) Lack of evidence for the toxic nectar hypothesis: a plant alkaloid did not deter nectar feeding by Lepidoptera. Fla Entomol 76:556–566

    CAS  Google Scholar 

  • Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K (2005) Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol Lett 8:1256–1263

    Google Scholar 

  • Leiss KA, Choi YH, Abdel-Farid IB, Verpoorte R, Klinkhamer PGL (2009) NMR metabolomics of thrips (Frankliniella occidentalis) resistance in Senecio hybrids. J Chem Ecol 35:219–229

    PubMed  CAS  Google Scholar 

  • Lindigkeit R, Biller A, Buch M, Schiebel HM, Boppre M, Hartmann T (1997) The two faces of pyrrolizidine alkaloids: the role of the tertiary amine and its N-oxide in chemical defense of insects with acquired plant alkaloids. Eur J Biochem 245:626–636

    PubMed  CAS  Google Scholar 

  • Loaiza JCM, Cespedes CL, Beuerle T, Theuring C, Hartmann T (2007) Ceroplastes albolineatus, the first scale insect shown to sequester pyrrolizidine alkaloids from its host-plant Pittocaulon praecox. Chemoecology 17:109–115

    CAS  Google Scholar 

  • Macel M (2010) Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phyrochem Rev. doi:10.1007/s11101-010-9181-1

  • Macel M, Klinkhamer PGL (2010) Chemotype of Senecio jacobaea affects damage by pathogens and insect herbivores in the field. Evol Ecol 24:237–250

    Google Scholar 

  • Macel M, Vrieling K (2003) Pyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae. J Chem Ecol 29:1435–1446

    PubMed  CAS  Google Scholar 

  • Macel M, Klinkhamer PGL, Vrieling K, Van Der Meijden E (2002) Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133:541–550

    Google Scholar 

  • Macel M, Bruinsma M, Dijkstra SM, Ooijendijk T, Niemeyer HM, Klinkhamer PGL (2005) Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. J Chem Ecol 31:1493–1508

    PubMed  CAS  Google Scholar 

  • Masters AR (1990) Pyrrolizidine alkaloids in artificial nectar protect adult ithomiine butterflies from spider predator. Biotropica 22:298–304

    Google Scholar 

  • Masters AR (1991) Dual role of pyrrolizidine alkaloids in nectar. J Chem Ecol 17:195–205

    CAS  Google Scholar 

  • Masters AR (1992) Chemical defense in Ithomiinae butterflies (Nymphalidae: Ithomiinae). PhD thesis, University of Florida

  • McLain DK (1984) Coevolution: müllerian mimicry between a plant bug (Miridae) and a seed bug (Lygaeidae) and the relationship between host plant choice and unpalatability. Oikos 43:143–148

    Google Scholar 

  • McLain DK, Shure DJ (1985) Host plant toxins and unpalatability of Neacoryphus bicrucis (Hemiptera: Lygaeidae). Ecol Entomol 10:291–298

    Google Scholar 

  • Meinwald J, Meinwald YC (1966) Strucuture and synthesis of the major component in the harir pencil secretion of a male butterfly, Lycorea ceres ceres (Cramer). J Am Chem Soc 86:1305–1310

    Google Scholar 

  • Narberhaus I, Zintgraf V, Dobler S (2005) Pyrrolizidine alkaloids on three trophic levels— evidence for toxic and deterrent effects on phytophages and predators. Chemoecology 15:121–125

    CAS  Google Scholar 

  • Naumann C, Hartmann T, Ober D (2002) Evolutionary recruitment of a flavin-dependent monooxygenase for the detoxification of host plant-acquired pyrrolizidine alkaloids in the alkaloid-defended arctiid moth Tyria jacobaeae. Proc Natl Acad Sci USA 99:6085–6090

    PubMed  CAS  Google Scholar 

  • Nickisch-Rosenegk E, Schneider D, Wink M (1990) Time-course of pyrrolizidine alkaloid processing in the alkaloid exploiting arctiid moth, Creatonotos transiens. Z Naturforsch 45c:881–894

    Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92

    PubMed  CAS  Google Scholar 

  • Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154

    CAS  Google Scholar 

  • Orr AG, Trigo JR, Witte L, Hartmann T (1996) Sequestration of pyrrolizidine alkaloids by larvae of Tellervo zoilus (Lepidoptera: Ithomiinae) and their role in the chemical protection of adults against the spider Nephila maculata (Araneidae). Chemoecology 7:68–73

    CAS  Google Scholar 

  • Pasteels JM, Hartmann T (2004) Sequestration of pyrrolizidine alkaloids in Oreina and Platyphora leaf beetles: physiological, ecological and evolutionary aspects. In: Jolivet P, Santiago-Blay JA, Schmitt M (eds) New developments in the biology of Chrysomelidae. SPB Academic Publishing, The Hague

    Google Scholar 

  • Patterson CG, Potter DA, Fannin FF (1991) Feeding deterrency of alkaloids from endophyte-infected grasses to japanese beetle grubs. Entomol Exp Appl 61:285–289

    CAS  Google Scholar 

  • Pelser PB, Gravendeel B, van der Meijden R (2002) Tackling speciose genera: species composition and phylogeny position of Senecio sect. Jacobaea (Asteraceae) based on plastid and nrDNA sequences. Am J Bot 89:929–939

    CAS  Google Scholar 

  • Pinheiro CEG (1996) Palatability and escaping ability in neotropical butterflies: experiments with wild kingbirds (Tyrannus melancholicus, Tyrannidae). Biol J Linn Soc 59:351–365

    Google Scholar 

  • Reinhard A, Janke M, von der Ohe W, Kempf M, Theuring C, Hartmann T, Schreier P, Beuerle T (2009) Feeding deterrence and detrimental effects of pyrrolizidine alkaloids fed to honey bees (Apis mellifera). J Chem Ecol 35:1086–1095

    PubMed  CAS  Google Scholar 

  • Rossini C, Hoebeke ER, Iyengar VK, Conner WE, Eisner M, Eisner T (2000) Alkaloid content of parasitois reared from pupae of an alkaloid-sequestering arctiid moth (Utetheisa ornatrix). Entomol News 111:287–290

    Google Scholar 

  • Rossini C, Bezzerides A, González A, Eisner M, Eisner T (2003) Chemical defense: incorporation of diet-derived pyrrolizidine alkaloid into the integumental scales of a moth (Utetheisa ornatrix). Chemoecology 13:199–205

    CAS  Google Scholar 

  • Rowell-Rahier M, Pasteels JM, Alonsomejia A, Brower LP (1995) Relative unpalatability of leaf beetles with either biosynthesized or sequestered chemical defense. Anim Behav 49:709–714

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis warning signals and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Schulz S (1998) Insect-plant interactions. Metabolism of plant compounds to pheromones and allomones by Lepidoptera and leaf beetles. Eur J Org Chem 1:13–20

    Google Scholar 

  • Schulz S (2009) Alkaloid-derived male courtship pheromones. In: Conner WE (ed) Tiger moths and woolly bears. Behaviour, ecology, and evolution of the Arctiidae. Oxford University Press, New York

    Google Scholar 

  • Schulz S, Beccaloni G, Brown KS, Boppré M, Freitas AVL, Ockenfels P, Trigo JR (2004) Semiochemicals derived from pyrrolizidine alkaloids in male ithomiine butterflies (Lepidoptera : Nymphalidae : Ithomiinae). Biochem Syst Ecol 32:699–713

    CAS  Google Scholar 

  • Silva KL, Trigo JR (2002) Structure-activity relationships of pyrrolizidine, alkaloids in insect chemical defense against the orb weaving spider Nephila clavipes. J Chem Ecol 28:657–668

    PubMed  CAS  Google Scholar 

  • Singer MS, Bernays EA (2009) Specialized generalist: behavioural and evolutionary ecology of polyphagous woolly bear caterpillars. In: Conner WE (ed) Tiger moths and woolly bears. Behaviour, ecology, and evolution of the Arctiidae. Oxford University Press, New York

    Google Scholar 

  • Singer MS, Carrière Y, Theuring C, Hartmann T (2004) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Am Nat 164:423–429

    PubMed  Google Scholar 

  • Speiser B, Harmatha J, Rowell-Raier M (1992) Effects of pyrrolizidine alkaloids and sesquiterpenes on snail feeding. Oecologia 92:257–265

    Google Scholar 

  • Thoden TC, Boppré M, Hallmann J (2009a) Effects of pyrrolizidine alkaloids on the performance of plant-parasitic and free-living nematodes. Pest Manag Sci 65:823–830

    PubMed  CAS  Google Scholar 

  • Thoden TC, Hallmann J, Boppré M (2009b) Effects of plants containing pyrrolizidine alkaloids on the northern root-knot nematode Meloidogyne hapla. Eur J Plant Pathol 123:27–36

    CAS  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Tinney G, Theuring C, Paul N, Hartmann T (1998) Effects of rust infection with Puccinia lagenophorae on pyrrolizidine alkaloids in Senecio vulgaris. Phytochemistry 49:1589–1592

    PubMed  CAS  Google Scholar 

  • Trigo JR (2000) The chemistry of antipredator defense by secondary compounds in Neotropical Lepidoptera: facts, perspectives and caveats. J Braz Chem Soc 11:551–561

    CAS  Google Scholar 

  • Trigo JR (2008) Chemical ecology of Ithomiine butterflies. In: Epifano F (ed) Current trends in phytochemistry. Research Signpost, Kerala

    Google Scholar 

  • Trigo JR, Brown KS, Witte L, Hartmann T, Ernst L, Barata LES (1996) Pyrrolizidine alkaloids: different acquisition and use patterns in Apocynaceae and Solanaceae feeding ithomiine butterflies (Lepidoptera: Nymphalidae). Biol J Linn Soc 58:99–123

    Google Scholar 

  • Trigo JR, Leal IR, Matzenbacher NI, Lewinsohn TM (2003) Chemotaxonomic value of pyrrolizidine alkaloids in southern Brazil Senecio (Senecioneae: Asteraceae). Biochem Syst Ecol 31:1011–1022

    CAS  Google Scholar 

  • Van Dam NM, Vuister LWN, Bergshoeff C, De Vos H, Van Der Meidjen E (1995) The “raison d’être” of pyrrolizidine alkaloids in Cynoglossum officinale: deterrent effects against generalist herbivores. J Chem Ecol 21:507–523

    Google Scholar 

  • Van Der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exp Appl 80:307–310

    Google Scholar 

  • Vasconcellos-Neto J, Lewinsohn TM (1984) Discrimination and release of unpalatable butterflies by Nephila clavipes, a neotropical orb-weaving spider. Ecol Entomol 9:337–344

    Google Scholar 

  • Vrieling K, van Wijk CAM (1994) Estimating costs and benefits of the pyrrolizidine alkaloids of Senecio jacobaea under natural conditions. Oikos 70:449–454

    CAS  Google Scholar 

  • Vrieling K, Soldaat LL, Smit W (1991) The influence of pyrrolizidine alkaloids of Senecio jacobaea on Tyria jacobaeae, Brachycaudus cardii and Haplothrips senecionis. Netherl J Zool 41:228–239

    Google Scholar 

  • Weller SJ, Jacobson NL, Conner WE (1999) The evolution of chemical defences and mating systems in tiger moths (Lepidoptera: Arctiidae). Biol J Linn Soc 68:557–578

    Google Scholar 

  • Witte L, Ehmke A, Hartmann T (1990) Interspecific flow of pyrrolizidine alkaloids—from plants via aphids to ladybirds. Naturwissenschaften 77:540–543

    CAS  Google Scholar 

  • Yosef R, Carrel JE, Eisner T (1996) Contrasting reactions of loggerhead shrikes to two types of chemically defended insect prey. J Chem Ecol 22:173–181

    CAS  Google Scholar 

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Acknowledgments

I acknowledge K. Leiss, H.K. Kim and P. Klinkhamer to invite me to review this fascinating subject. I thank D. Rodrigues, M. Pareja, K. Leiss, and three anonymous reviewers for their comments on the manuscript and their assistance with the English language. L. Kaminski kindly drew the figures. This review was supported by CNPq grant (304473/2009-0).

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  1. Laboratório de Ecologia Química, Departamento de Biologia Animal, Instituto de Biologia, Unicamp, CP 6109, Campinas, SP, 13083-970, Brazil

    José Roberto Trigo

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Trigo, J.R. Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10, 83–98 (2011). https://doi.org/10.1007/s11101-010-9191-z

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