Abstract
The evolution of the diversity in plant secondary compounds is often thought to be driven by insect herbivores, although there is little empirical evidence for this assumption. To investigate whether generalist insect herbivores could play a role in the evolution of the diversity of related compounds, we examined if (1) related compounds differ in their effects on generalists, (2) there is a synergistic effect among compounds, and (3) effects of related compounds differed among insect species. The effects of pyrrolizidine alkaloids (PAs) were tested on five generalist insect herbivore species of several genera using artificial diets or neutral substrates to which PAs were added. We found evidence that structurally related PAs differed in their effects to the thrips Frankliniella occidentalis, the aphid Myzus persicae, and the locust Locusta migratoria. The individual PAs had no effect on Spodoptera exigua and Mamestra brassicae caterpillars. For S. exigua, we found indications for synergistic deterrent effects of PAs in PA mixtures. The relative effects of PAs differed between insect species. The PA senkirkine had the strongest effect on the thrips, but had no effect at all on the aphids. Our results show that generalist herbivores could potentially play a role in the evolution and maintenance of the diversity of PAs.
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References
C. Adams E. Bernays (1978) ArticleTitleThe effects of combinations of deterrents on the feeding behavior of Locusta migratoria Entomol. Exp. Appl. 23 101–109 Occurrence Handle1:CAS:528:DyaE1cXlt1Cmsrs%3D
A. A. Agrawal (2000) ArticleTitleBenefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae) Ecology 81 1804–1813
M. D. Bentley D. E. Leonard W. F. Stoddard L. H. Zalkow (1984) ArticleTitlePyrrolizidine alkaloids as larval feeding deterrents for spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae) Ann. Entomol. Soc. Am. 77 393–397 Occurrence Handle1:CAS:528:DyaL2cXlsVKjurs%3D
M. Berenbaum P. Feeny (1981) ArticleTitleToxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? Science 212 927–929 Occurrence Handle1:CAS:528:DyaL3MXktF2gsbg%3D
M. Berenbaum A. R. Zangerl J. K. Nitao (1986) ArticleTitleConstraints on chemical coevolution: wild parsnips and the parsnip webworm Evolution 40 1215–1228 Occurrence Handle1:CAS:528:DyaL2sXjtVWmuw%3D%3D
M. Berenbaum A. R. Zangerl K. Lee (1989) ArticleTitleChemical barriers to adaptation by a specialist herbivore Oecologia 18 586–608
M. Berenbaum J. K. Nitao A. R. Zangerl (1991) ArticleTitleAdaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae) J. Chem. Ecol. 17 207–215 Occurrence Handle1:CAS:528:DyaK3MXhtFymt7w%3D
M. D. Bowers G. M. Puttick (1988) ArticleTitleResponse of generalist and specialist insects to qualitative allelochemical variation J. Chem. Ecol. 14 319–334 Occurrence Handle1:CAS:528:DyaL1cXht1yqt7c%3D
L. B. Bull C. C. J. Culvenor A. T. Dick (1968) The Pyrrolizidine Alkaloids: Their Chemistry, Pathogenicity and Other Biological Properties John Wiley & Sons Inc. New York
R. H. Dadd T. E. Mittler (1966) ArticleTitlePermanent culture of an aphid on a totally synthetic diet Experientia 22 832–833 Occurrence Handle1:CAS:528:DyaF2sXksVKgsw%3D%3D Occurrence Handle5973229
N. J. De Boer Particlede (1999) ArticleTitlePyrrolizidine alkaloid distribution in Senecio jacobaea minimises losses to generalist feeding Entomol. Exp. Appl. 91 169–173 Occurrence Handle1:CAS:528:DyaK1MXmsFGmu7c%3D
C. M. De Jager Particlede R. P. T. BÛtot E. Van Der Meijden Particlevan der R. Verpoorte (1996) ArticleTitleThe role of primary and secondary metabolites in chrysanthemum resistance to Frankliniella occidentalis J. Chem. Ecol. 22 1987–1999 Occurrence Handle1:CAS:528:DyaK28XnsVWku7c%3D
S. Dobler (2001) ArticleTitleEvolutionary aspects of defense by recycled plant compounds Basic Appl. Ecol. 2 15–26 Occurrence Handle1:CAS:528:DC%2BD3MXktF2lu78%3D
D. L. Dreyer K. C. Jones R. J. Molyneux (1985) ArticleTitleFeeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrthosiphon pisum) and evidence for phloem transport of indolizidine alkaloid swaisonine J. Chem. Ecol. 11 1045–1051 Occurrence Handle1:CAS:528:DyaL2MXltl2jtrc%3D
P. R. Ehrlich P. H. Raven (1964) ArticleTitleButterflies and plants: a study in coevolution Evolution 18 586–608
P. Feeny (1976) ArticleTitlePlant apparency and chemical defense Recent Adv. Phytochem. 10 1–40 Occurrence Handle1:CAS:528:DyaE2sXhvVGrtrw%3D
G. A. Fox (1993) Failure-time analysis: emergence, flowering, survivorship, and other waiting times S. M. Scheiner J. Gurevitch (Eds) Design and Analysis of Ecological Experiments Chapman and Hall New York 253–289
H. Frei J. LÜthy J. Brauchli U. Zweifel F. E. WÜrgler C. Schlatter (1992) ArticleTitleStructure/activity relationships of the genotoxic potencies of sixteen pyrrolizidine alkaloids assayed for the induction of somatic mutation and recombination in wing cells of Drosophila melanogaster Chem. Biol. Interactions 83 1–22 Occurrence Handle1:CAS:528:DyaK38Xks1ClsLk%3D
B. F. HÄgele M. Rowell-Rahier (2000) ArticleTitleChoice, 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
T. Hartmann (1999) ArticleTitleChemical ecology of pyrrolizidine alkaloids Planta 207 483–495 Occurrence Handle1:CAS:528:DyaK1MXhslKisrg%3D
T. Hartmann B. Dierich (1998) ArticleTitleChemical diversity and variation of pyrrolizidine alkaloids of the senecionine type: Biological need or coincidence? Planta 206 443–451 Occurrence Handle1:CAS:528:DyaK1cXlvVeisr8%3D
T. Hartmann G. Toppel (1987) ArticleTitleSenecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures of Senecio vulgaris Phytochemistry 26 1639–1643 Occurrence Handle1:CAS:528:DyaL2sXksFGrs7w%3D
T. Hartmann L. Witte (1995) Chemistry, biology and chemoecology of the pyrrolizidine alkaloids S. W. Pelletier (Eds) Alkaloids: Chemical and Biological Perspectives, Vol. 9 Pergamon Press Elmsford, New York 156–233
T. Hartmann M. Zimmer (1986) ArticleTitleOrgan-specific distribution and accumulation of pyrrolizidine alkaloids during the life history of two annual Senecio species J. Plant Physiol. 122 67–80 Occurrence Handle1:CAS:528:DyaL28Xhs1GgtL8%3D
W. H. G. Hol J. A. Van Veen Particlevan (2002) ArticleTitlePyrrolizidine alkaloids from Senecio jacobaea affect fungal growth J. Chem. Ecol. 28 1751–1760
K. S. Johnson J. M. Scriber M. Nair (1996) ArticleTitlePhenylpropenoid phenolics in sweetbay magnolia as chemical determinants of host use in saturniid silkmoths (Callosamia) J. Chem. Ecol. 22 1955–1969 Occurrence Handle1:CAS:528:DyaK28XnsVWku70%3D
T. Juenger J. Bergelson (1998) ArticleTitlePairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata Evolution 52 1583–1592
D. J. Kliebenstein J. Kroymann P. Brown A. Figuth D. Pedersen J. Gershenzon T. Mitchell-Olds (2001) ArticleTitleGenetic control of natural variation in Arabidopsis glucosinolate accumulation Plant Physiol. 126 811–825 Occurrence Handle1:CAS:528:DC%2BD3MXks1GmsL4%3D Occurrence Handle11402209
Y. B. Linhart (1991) ArticleTitleDisease, parasitism and herbivory: Multidimensional challenges in plant evolution Trends Ecol. Evol. 6 392–396
R. L. Lindroth J. M. Scriber S. M. T. Hsia (1988) ArticleTitleChemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides Ecology 69 814–822 Occurrence Handle1:CAS:528:DyaL1cXkvFSjt7c%3D
M. Macel K. Vrieling (2003) ArticleTitlePyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae J. Chem. Ecol. 29 1435–1446 Occurrence Handle1:CAS:528:DC%2BD3sXksF2jsbw%3D Occurrence Handle12918926
M. Macel P. G. L. Klinkhamer K. Vrieling E. Van Der Meijden Particlevan der (2002) ArticleTitleDiversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae Oecologia 133 541–550
M. Macel K. Vrieling P. G. L. Klinkhamer (2004) ArticleTitleVariation in pyrrolizidine alkaloid patterns of Senecio jacobaea Phytochemistry 65 865–873 Occurrence Handle1:CAS:528:DC%2BD2cXjtVOis7s%3D Occurrence Handle15081286
A. R. Mattocks (1968) ArticleTitleToxicity of pyrrolizidine alkaloids Nature 217 723–728 Occurrence Handle1:CAS:528:DyaF1cXosFOqtA%3D%3D Occurrence Handle5641123
R. Mauricio M. D. Rausher (1997) ArticleTitleExperimental manipulation of putative selection agents provides evidence for the role of natural enemies in the evolution of plant defense Evolution 51 1435–1444
B. Mersey A. Cutler (1986) ArticleTitleDifferential distribution of specific indole alkaloids in leaves of Catharanthus roseus Can. J. Bot. 64 1039–1045 Occurrence Handle1:CAS:528:DyaL28XkslGqtrg%3D
J. S. Miller P. Feeny (1983) ArticleTitleEffects of benzylisoquinoline alkaloids on the larvae of polyphagous Lepidoptera Oecologia 58 332–339
R. Mithen A. F. Raybould A. Giamoustaris (1995) ArticleTitleDivergent selection for secondary metabolites between wild populations of Brassica oleracea and its implications for plant–herbivore interactions Heredity 75 472–484 Occurrence Handle1:CAS:528:DyaK28XisFGhtA%3D%3D
C. Naumann T. Hartmann D. Ober (2002) ArticleTitleEvolutionary 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 Occurrence Handle1:CAS:528:DC%2BD38XjslWnsrw%3D Occurrence Handle11972041
J. M. Pasteels C. Theuring L. Witte T. Hartmann (2003) ArticleTitleSequestration and metabolism of prototoxic pyrrolizidine alkaloids by larvae of the leaf beetle Platyphora boucardi and their transfer via pae into defensive secretions of adults J. Chem. Ecol. 29 337–355 Occurrence Handle1:CAS:528:DC%2BD3sXhs1CrtbY%3D Occurrence Handle12737262
D. F. Rhoades R. G. Cates (1976) ArticleTitleToward a general theory of plant antiherbivore chemistry Recent Adv. Phytochem. 10 168–213 Occurrence Handle1:CAS:528:DyaE2sXhvVGrtr0%3D
J. E. Rodman (1981) Divergence, convergence and parallelism in phytochemical characters: The glucosinolate–myrosinase system D. A. Young D. S. Seigler (Eds) Phytochemistry and Angiosperm Phylogeny Praeger Publishers New York 43–79
M. Rothschild R. T. Aplin P. A. Cockrum J. A. Edgar P. Fairweather R. Lees (1979) ArticleTitlePyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of these secondary substances in the Arctiidae Biol. J. Linn. Soc. 12 305–326
I. Shonle J. Bergelson (2000) ArticleTitleEvolutionary ecology of the tropane alkaloids of Datura stramonium L. (Solanaceae) Evolution 54 778–788 Occurrence Handle1:CAS:528:DC%2BD3cXlsVSnurg%3D Occurrence Handle10937252
E. L. Simms (1990) ArticleTitleExamining selection on the multivariate phenotype: Plant resistance to herbivores Evolution 44 1177–1188
P. Singh (1983) ArticleTitleA general purpose laboratory diet mixture for rearing insects Insect Sci. Appl. 4 357–362
N. M. Van Dam Particlevan L. W. N. Vuister C. Bergshoeff H. De Vos Particlede E. Van Der Meijden Particlevan der (1995) ArticleTitleThe ‘raison d’être’ of pyrrolizidine alkaloids in Cynoglossum officinale: Deterrent effects against generalist herbivores J. Chem. Ecol. 21 507–523 Occurrence Handle1:CAS:528:DyaK2MXmt1Sgu7Y%3D
N. M. Van Dam Particlevan T. J. De Jong Particlede Y. Iwasa T. Kubo (1996) ArticleTitleOptimal distribution of defenses: are plants smart investors? Funct. Ecol. 10 128–136
E. Van Der Meijden Particlevan der (1996) ArticleTitlePlant defence, an evolutionary dilemma: Contrasting effects of (specialist and generalist) herbivores and natural enemies Entomol. Exp. Appl. 80 307–310
K. Vrieling H. De Vos Particlede C. A. M. Van Wijk Particlevan (1993) ArticleTitleGenetic analysis of the concentration of pyrrolizidine alkaloids of Senecio jacobaea Phytochemistry 32 1141–1144 Occurrence Handle1:CAS:528:DyaK3sXitlSgtrk%3D
L. Witte L. Ernst H. Adam T. Hartmann (1992) ArticleTitleChemotypes of two pyrrolizidine alkaloid-containing Senecio species Phytochemistry 31 559–565 Occurrence Handle1:CAS:528:DyaK38XlsVOit7Y%3D
A. R. Zangerl F. A. Bazzaz (1992) Theory and pattern in plant defense allocation R. S. Fritz E. L. Simms (Eds) Plant Resistance to Herbivores and Pathogens University of Chicago Press Chicago 363–391
Acknowledgments
This research was supported by a grant from the Gratama foundation. We thank Helene de Vos for the isolation of jacobine, Lily Muñoz, Henk Nell, and Kees Koops for their technical assistance, Leo Koopman for providing the Mamestra, and Klaas Vrieling, Nicole van Dam, and Ed van der Meijden for their valuable comments on earlier drafts of the manuscript.
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Macel, M., Bruinsma, M., Dijkstra, S.M. et al. Differences in Effects of Pyrrolizidine Alkaloids on Five Generalist Insect Herbivore Species. J Chem Ecol 31, 1493–1508 (2005). https://doi.org/10.1007/s10886-005-5793-0
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DOI: https://doi.org/10.1007/s10886-005-5793-0