Abstract
Plants produce a variety of secondary metabolites that function as a defense against their natural enemies. Production of these secondary metabolites is genetically controlled, but is also phenotypically plastic and varies in response to both biotic and abiotic factors. Therefore, plant species may vary widely in their chemical defenses and such variation can be evident at temporal, spatial and tissue levels. Focusing on the chemical defenses of a native Colorado wildflower, Penstemon virgatus, we assessed the variation in iridoid glycoside (IG) content across two non-consecutive growing seasons, six natural populations and three tissue types: leaves, stems and flowers. Our results indicate that P. virgatus plants contain high concentrations of IGs (mean = 23.36% dry weight of leaves) and that IGs were differentially allocated among tissue types. Leaves contained the highest concentration of IGs, which varied quantitatively between sampling years, among plant populations, and plant parts. We also quantified leaf herbivore damage at all six populations but we found very little herbivore damage. Our study indicates that the IG concentrations of P. virgatus plants are both spatially and temporally variable. Furthermore, the high concentrations of secondary metabolites combined with the low levels of damage suggest that these plants are well defended against generalist herbivores.
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References
Adler FR, Karban R (1994) Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am Nat 144(5):813–832
Alba C, Prioreschi R, Quintero C (2013) Population and leaf-level variation of iridoid glycosides in the invasive weed Verbascum thapsus L (common mullein): implications for herbivory by generalist insects. Chemoecology 23(2):83–92
Berenbaum MR, Zangerl AR, Nitao JK (1986) Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40(6):1215–1228
Boros CA, Stermitz FR (1990) Iridoids an updated review part I. J Nat Prod 53:1055–1147
Bowers MD, Collinge SK (1992) Fate of iridoid glycosides in different life stages of the buckeye Junonia coenia (Lepidoptera Nymphalidae). J Chem Ecol 18:817–831
Bowers MD, Puttick GM (1988) Response of generalist and specialist insects to qualitative allelochemical variation. J Chem Ecol 14:319–334
Bowers MD, Stamp NE (1992) Chemical variation with and between individuals of Plantago laceolata. J Chem Ecol 18:989–995
Brenes-Arguedas T, Coley PD (2005) Phenotypic variation and spatial structure of secondary chemistry in a natural population of a tropical tree species. Oikos 108:410–420
Cirak C, Radusiene J, Stanius Z, Camas N, Caliskan O, Serhat Odobas M (2012) Secondary metabolites of Hypericum orientale L growing in Turkey: variation among populations and plant parts. Acta Physiol Plant 34:1313–1320
Crosswhite FS (1967) Revision of Penstemon section Habroanthus (Scrophulariaceae) III: series Virgati. Am Midl Nat 77:28–41
Darrow K, Bowers MD (1997) Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem Syst Ecol 25:1–11
Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398
Fajer ED, Bowers MD, Bazzaz FA (1992) The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago – a test of the carbon nutrient balance hypothesis. Am Nat 140:707–723
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(1):23–29
Fortuna TM, Eckert S, Harvey JA, Vet LE, Müller C, Gols R (2014) Variation in plant defences among populations of a range - expanding plant: consequences for trophic interactions. New Phytol 204(4):989–999
Gardner DR, Stermitz FR (1988) Host Plant Utilization and Iridoid Glycoside Sequestration by Euphydryas anicia (Lepidoptera Nymphalidae). J Chem Ecol 14:2147–2168
Gols R, Raaijmakers CE, van Dam NM, Dicke M, Bukovinszky T, Harvey JA (2007) Temporal changes affect plant chemistry and tritrophic interactions. Basic Appl Ecol 8:421–433
Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA (2008) Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89:1616–1626
Gols R, van Dam NM, Raaijmakers CE, Dicke M, Harvey JA (2009) Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps? Oikos 118:733–743
Gouyon PH, Fort PH, Caraux G (1983) Selection of seedlings of Thymus vulgaris by grazing slugs. J Ecol 73:299–306
Harper JL (1977) Population biology of plants. Academic Press, London
Harper JL, White J (1974) The demography of plants. Annu rev Ecol Syst 5:419–463
Jamieson MA, Bowers MD (2010) Iridoid glycoside variation in the invasive plant Dalmatian toadflax Linaria dalmatica (Plantaginaceae) and sequestration by the biological control agent Calophasia lunula. J Chem Ecol 36:70–79
Kelly CA, Bowers MD (2016) Preference and performance of generalist and specialist herbivores on chemically defended host plants. Exol Entomol 41(3):308–316
Krischik VA, Denno RF (1983) Individual population and geographic patterns in plant defense. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 463–512
L’Empereur KM (1989) Iridoid glycoside and pyrrolizidine alkaloid sequestration by specialist Lepidoptera. Colorado State University, Dissertation
L’Empereur KM, Stermitz FR (1990a) Iridoid glycoside content of Euphydryas anicia (Lepidoptera: Nymphalidae) and its major host plant Besseya plantaginea (Scrophulariaceae) at a high plains Colorado site. J Chem Ecol 16:187–197
L’Empereur KM, Stermitz FR (1990b) Iridoid glycoside metabolism and sequestration by Poladryas minuta (Lepidoptera: Nymphalidae) feeding on Penstemon virgatus (Scrophulariaceae). J Chem Ecol 16:1495–1506
Laitinen ML, Julkunen-Tiitto R, Tahvanainen J, Heinonen J, Rousi M (2005) Variation in birch (Betula pendula) shoot secondary chemistry due to genotype environment and ontogeny. J Chem Ecol 31:697–717
Martins CHZ, Cunha BP, Solferini VN, Trigo JR (2015) Feeding on host plants with different concentrations and structures of pyrrolizidine alkaloids impacts the chemical-defense effectiveness of a specialist herbivore. PLoS One 10:e0141480
McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98(5):985–992
McKey D (1979) The distribution of secondary compounds within plants in: Rosenthal GA, Janzen DH (eds) herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 55–133
Mody K, Unsicker SB, Linsenmair KE (2007) Fitness related diet-mixing by intrapsecific host – plant - switching of specialist insect herbivores. Ecology 88(4):1012–1020
Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201(3):733–750
Moyes CL, Collin HA, Britton G, Raybould AF (2000) Glucosinolates and differential herbivory in wild populations of Brassica oleracea. J Chem Ecol 26(11):2625–2641
Murphy DD, Wahlberg N, Hanski I, Ehrlich PR (2004) Introducing checkerspots: taxonomy and ecology. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, New York, pp 17–33
Newton EL, Bullock JM, Hodgson DJ (2009a) Bottom-up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations. Ecol Entomol 34:614–623
Newton EL, Bullock JM, Hodgson DJ (2009b) Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76
Nichols-Orians CM (1991) Environmentally induced differences in plant traits: consequences for susceptibility to a leaf-cutter ant. Ecology 72:1609–1623
Pankoke H, Buschmann T, Müller C (2013) Role of plant β-glucosidases in the dual defense system of iridoid glycosides and their hydrolyzing enzymes in Plantago lanceolata and Plantago major. Phytochemistry 94:99–107
Puttick GM, Bowers MD (1988) Effect of qualitative and quantitative variation in allelochemicals on a generalist insect: Iridoid glycosides and the southern armyworm. J Chem Ecol 14:335–351
Quintero C, Bowers MD (2011) Plant induced defenses depend more on plant age than previous history of damage: implications for plant-herbivore interactions. J Chem Ecol 37:992–1001
Quintero C, Bowers MD (2012) Changes in plant chemical defences and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae). Oecologia 168:471–481
Quintero C, Bowers MD (2013) Effects of insect herbivory on induced chemical defences and compensation during early plant development in Penstemon virgatus. Ann bot-London 112:661–669
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Rios RS, Marquis RJ, Flunker JC (2008) Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata (Fabaceae). Oecologia 156:577–588
Roach DA, Gampe J (2004) Age - specific demography in Plantago: uncovering age - dependent mortality in a natural population. Am Nat 164:60–69
Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernandez LM (2002) Hostplants of the moth and butterfly caterpillars of America north of Mexico. Mem am Entomol Inst 69:1–824
Safranyik L, Carroll AL (2006) The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In: Safranyik L, Wilson B (eds) The mountain pine beetle: a synthesis of its biology management and impacts on Lodgepole pine. Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, Victoria, pp 3–66
Scogings PF, Dziba LE, Gordon IJ (2004) Leaf chemistry of woody plants in relation to season canopy retention and goat browsing in a semiarid subtropical savanna. Austral Ecol 29:278–286
Shonle I, Klett JE, Vickerman LG (2004) Native herbaceous perennials for Colorado landscapes. Colorado State University Cooperative Extension http://extension.colostate.edu/topic-areas/yard-garden/native-herbaceous-perennials-for-colorado-landscapes-7-242/. Accessed 20 Dec 2016
Small EE, Larson KM, Braun JJ (2010) Sensing vegetation growth with reflected GPS signals. Geophys res Lett 37:L12401
Smallegange RC, van Loon JJA, Blatt SE, Harvey JA, Agerbirk N, Dicke M (2007) Flower vs. leaf feeding by Pieris brassicae: Glucosinolate-rich flower tissues are preferred and sustain higher growth rate. J Chem Ecol 33:1831–1844
Sourakov A (2015) You are what you eat: native versus exotic Crotalaria species (Fabaceae) as host plants of the ornate Bella moth Utetheisa ornatrix (Lepidoptera: Erebidae: Arctiinae). J Nat Hist 49:2397–2415
Stamp NE (2003) Theory of plant defensive level: example of process and pitfalls in development of ecological theory. Oikos 102:672–678
Stamp NE, Bowers MD (1996) Consequences for plantain chemistry and growth when herbivores are attacked by predators. Ecology 77:535–549
Stermitz FR, Gardner DR, McFarland N (1988) Iridoid glycoside sequestration by two aposematic Penstemon-feeding geometrid larvae. J Chem Ecol 14:435–441
Strauss SY, Irwin RE, Lambrix VM (2004) Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J Ecol 92:132–141
Uvarov B (1977) Grasshoppers and locusts. A handbook of general Acridology. Vol. 2. Behaviour, ecology, biogeography, population dynamics. Centre for Overseas Pest Research, London
Wallin KF, Raffa KF (2004) Feedback between individual host selection behavior and population dynamics in an eruptive herbivore. Ecol Monogr 74:101–116
Waterman PG, Mole S (1989) Extrinsic factors influencing production of secondary metabolites in plants. In: Bernays EA (ed) Insect-plant interactions. CRC Press, Boca Raton, pp 107–134
Wilson LM, Sing SE, Piper GL, Hansen RW, De Clerck-Floate R, MacKinnon DK, C Randall (2005) Biology and Biological Control of Dalmatian and Yellow Toadflax. USDA Forest Service, FHTET-05-13
Acknowledgments
We thank Farah Abdelmawla, Michael Belazis, Hadley Hanson, Jason Hong, Quinn Langsfeld, Gift Pornsawan Poopat and Kristin White for field and laboratory assistance. We gratefully acknowledge Carolina Quintero, the members of the Bowers lab and Zachary Mullen for valuable feedback on experimental design and statistical analysis. We also thank P. Molgaard (University of Copenhagen) for providing standards of scutellarioside. This work was supported by grants from the Undergraduate Research Opportunity Program (to MDB), the Department of Ecology and Evolutionary Biology at the University of Colorado, Boulder (to CAK), the John W. Marr Fund in Plant Ecology (to CAK), the Hazel Schmoll Award (to CAK) and the William H. Burt Award (to CAK).
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Kelly, C.A., Bowers, M. The Perennial Penstemon: Variation in Defensive Chemistry Across Years, Populations, and Tissues. J Chem Ecol 43, 599–607 (2017). https://doi.org/10.1007/s10886-017-0854-8
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DOI: https://doi.org/10.1007/s10886-017-0854-8