Nitrogen enrichment differentially affects above- and belowground plant defense

American Journal of Botany

Volumn 99, Issue 10, 2012, Pages 1630-1637

  Jamieson, Mary A ^a,b   Seastedt, Timothy R ^a   Deane Bowers, M ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Defense costs; Growth differentiation balance hypothesis; Invasive plant; Iridoid glycosides; Linaria dalmatica; Nitrogen deposition; Optimal defense hypothesis; Resource allocation; Root defense; Secondary metabolites

Indexed keywords

IRIDOID; NITROGEN; PHEROMONE;

GROWTH RATE; HERB; INVASIVE SPECIES; NITROGEN; PLANT DEFENSE; RESOURCE ALLOCATION; SECONDARY METABOLITE; TERRESTRIAL ECOSYSTEM;

ARTICLE; BIOLOGICAL MODEL; BIOMASS; CHEMISTRY; FLOWER; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; LINARIA; METABOLISM; SOIL;

BIOMASS; FLOWERS; HUMANS; IRIDOID GLYCOSIDES; LINARIA; MODELS, BIOLOGICAL; NITROGEN; PHEROMONES; SOIL;

EID: 84867617134     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100492     Document Type: Article

References (68)

1. AERTS, R., AND F. S. CHAPIN. 2000. The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. Advances in Ecological Research 30: 1-67.
2. BARTON, K. E., AND J. KORICHEVA. 2010. The ontogeny of plant defense and herbivory: Characterizing general patterns using meta-analysis. American Naturalist 175: 481-493.
3. BAZZAZ, F. A., N. R. CHIARIELLO, P. D. COLEY, AND L. F. PITELKA. 1987. Allocating resources to reproduction and cefense. BioScience 37: 58-67.
4. BENINGER, C. W., R. R. CLOUTIER, AND B. GRODZINSKI. 2008. The iridoid glucoside, antirrhinoside, from Antirrhinum majus L. has differential effects on two generalist insect herbivores. Journal of Chemical Ecology 34: 591-600.
5. BENINGER, C. W., R. R. CLOUTIER, AND B. GRODZINSKI. 2009. A comparison of antirrhinoside distribution in the organs of two related Plantaginaceae species with different reproductive strategies. Journal of Chemical Ecology 35: 1363-1372.
6. BENINGER, C. W., R. R. CLOUTIER, M. A. MONTEIRO, AND B. GRODZINSKI. 2007. The distribution of two major iridoids in different organs of Antirrhinum majus L. at selected stages of development. Journal of Chemical Ecology 33: 731-747.
7. BEZEMER, T. M., AND N. M. VAN DAM. 2005. Linking aboveground and belowground interactions via induced plant defenses. Trends in Ecology & Evolution 20: 617-624.
8. BIERE, A., H. B. MARAK, AND J. M. M. V AN DAMME. 2004. Plant chemical defense against herbivores and pathogens: Generalized defense or trade-offs? Oecologia 140: 430-441.
9. BLUMENTHAL, D. M. 2006. Interactions between resource availability and enemy release in plant invasion. Ecology Letters 9: 887-895.
10. BOEGE, K., AND R. J. MARQUIS. 2005. Facing herbivory as you grow up: The ontogeny of resistance in plants. Trends in Ecology & Evolution 20: 441-448.
11. BOROS, C. A., AND F. R. STERMITZ. 1990. Iridoids. An Updated Review. Part I. Journal of Natural Products 53: 1055-1147.
12. BOROS, C. A., AND F. R. STERMITZ. 1991. Iridoids. An Updated Review. Part 2. Journal of Natural Products 54: 1173-1246.
13. BOWERS, M. D. 1991. Iridoid glycosides. In G. A. Rosenthal and M. R. Berenbaum [eds.], Herbivores: their interactions with secondary plant metabolites, 297-326. Academic Press, New York, New York, USA.
14. BOWERS, M. D., AND N. E. STAMP. 1993. Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74: 1778-1791.
15. BURKE, I. C., W. K. LAUENROTH, AND W. J. PARTON. 1997. Regional and temporal variation in net primary production and nitrogen mineralization in grasslands. Ecology 78: 1330-1340.
16. CAPPUCCINO, N., AND J. T. ARNASON. 2006. Novel chemistry of invasive exotic plants. Biology Letters 2: 189-193.
17. CHAPIN, F. S., III, A. J. BLOOM, C. B. FIELD, AND R. H. WARING. 1987. Plant responses to multiple environmental factors. BioScience 37: 49-57.
18. COLEY, P. D., J. P. BRYANT, AND F. S. CHAPIN. 1985. Resource availability and plant antiherbivore defense. Science 230: 895-899.
19. DAEHLER, C. C. 2003. Performance comparisons of co-occurring native and alien invasive plants: Implications for conservation and restoration. Annual Review of Ecology Evolution and Systematics 34: 183-211.
20. DARROW, K., AND M. D. BOWERS. 1999. Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. Journal of Chemical Ecology 25: 1427-1440
21. DE DEYN, G. B., A. BIERE, W. H. VAN DER PUTTEN, R. WAGENAAR, AND J. N. KLIRONOMOS. 2009. Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia 160: 433-442.
22. DUNCAN, C. A., J. J. JACHETTA, M. L. BROWN, V. F. CARRITHERS, J. K. CLARK, J. M. DITOMASO, R. G. LYM, ET AL. 2004. Assessing the economic, environmental, and societal losses from invasive plants on rangeland and wildlands. Weed Technology 18: 1411-1416.
23. FENN, M. E., R. HAEUBER, G. S. TONNESEN, J. S. BARON, S. GROSSMANCLARKE, D. HOPE, D. A. JAFFE, ET AL. 2003. Nitrogen emissions, deposition, and monitoring in the western United States. Bioscience 53: 391-403.
24. FONTANA, A., M. REICHELT, S. HEMPEL, J. GERSHENZON, AND S. B. UNSICKER. 2009. The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. Journal of Chemical Ecology 35: 833-843.
25. FRANZYK, H., S. R. J ENSEN, Z. T HALE, AND C. E. OLSEN. 1999. Halohydrins and polyols derived from antirrhinoside: Structural revisions of muralioside and epimuralioside. Journal of Natural Products 62: 275-278.
26. GALLOWAY, J. N., F. J. DENTENER, D. G. CAPONE, E. W. BOYER, R. W. HOWARTH, S. P. SEITZINGER, G. P. ASNER, ET AL. 2004. Nitrogen cycles: Past, present, and future. Biogeochemistry 70: 153-226.
27. GARDNER, D. R., AND F. R. STERMITZ. 1988. Host plant utilization and iridoid glycoside sequestration by Euphydryas anicia (Lepidoptera, Nymplalidae). Journal of Chemical Ecology 14: 2147-2168.
28. GOWAN, E., B. A. LEWIS, AND R. TURGEON. 1995. Phloem transport of antirrhinoside, an iridoid glycoside, in Asarina scandens (Scrophulariaceae). Journal of Chemical Ecology 21: 1781-1788.
29. GRÖGER, D., AND S. J OHNE. 1 965. Ü ber das vorkommen von peganin in Linaria arten. Planta Medica 13: 182-188.
30. GUSEWELL, S. 2004. N:P ratios in terrestrial plants: Variation and functional signifi cance. New Phytologist 164: 243-266.
31. HAASE, D. L., AND R. ROSE. 1995. Vector analysis and its use for interpreting plant nutrient shifts in response to silvicultural treatments. Forest Science 41: 54-66.
32. HAMILTON, J. G., A. R. ZANGERL, E. H. DELUCIA, AND M. R. BERENBAUM. 2001. The carbon-nutrient balance hypothesis: Its rise and fall. Ecology Letters 4: 86-95.
33. HANDJIEVA, N. V., E. I. ILIEVA, S. L. SPASSOV, S. S. POPOV, AND H. DUDDECK. 1993. Iridoid glycosides from Linaria species. Tetrahedron 49: 9261-9266.
34. HERMS, D. A., AND W. J. MATTSON. 1992. The dilemma of plants-to grow or defend. Quarterly Review of Biology 67: 283-335.
35. JAMIESON, M. A., AND M. D. B OWERS. 2010. Iridoid glycoside variation in the invasive plant Dalmatian toadfl ax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula. Journal of Chemical Ecology 36: 70-79.
36. JAMIESON, M. A., AND M. D. BOWERS. 2012a. Plant-mediated effects of soil nitrogen enrichment on a chemically defended specialist herbivore, Calophasia lunula. Ecological Entomology 37: 300-308.
37. JAMIESON, M. A., AND M. D. BOWERS. 2012b. Soil nitrogen availability and herbivore attack infl uence the chemical defenses of an invasive plant (Linaria dalmatica; Plantaginaceae). Chemoecology 22: 1-11.
38. JAMIESON, M. A., D. KNOCHEL, A. MANRIQUE, AND T. R. SEASTEDT. 2012. Top-down and bottom-up controls on Dalmatian toadfl ax (Linaria dalmatica) performance along the Colorado Front Range, USA. Plant Ecology 213: 185-195.
39. JARZOMSKI, C. M., N. E. STAMP, AND M. D. BOWERS. 2000. Effects of plant phenology, nutrients and herbivory on growth and defensive chemistry of plantain, Plantago lanceolata. Oikos 88: 371-379.
40. KAPLAN, I., R. HALITSCHKE, A. KESSLER, S. SARDANELLI, AND R. F. DENNO. 2008. Constitutive and induced defenses to herbivory in above-and belowground plant tissues. Ecology 89: 392-406.
41. KORICHEVA, J. 1999. Interpreting phenotypic variation in plant allelochemistry: Problems with the use of concentrations. Oecologia 119: 467-473.
42. KORICHEVA, J. 2002. Meta-analysis of sources of variation in fi tness costs of plant antiherbivore defenses. Ecology 83: 176-190.
43. KORICHEVA, J., S. LARSSON, E. HAUKIOJA, AND M. KEINANEN. 1998. Regulation of woody plant secondary metabolism by resource availability: Hypothesis testing by means of meta-analysis. Oikos 83: 212-226.
44. LOGAN, B. A., B. DEMMIG-ADAMS, T. H. ROSENSTIEL, AND W. W. ADAMS. 1999. Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209: 213-220.
45. LOOMIS, W. E. 1932. Growth-differentiation balance vs carbohydratenitrogen ratio. Proceedings of the American Society for Horticultural Sciences: 240-245.
46. MARAK, H. B., A. BIERE, AND J. M. M. VAN DAMME. 2002. Systemic, genotype-specifi c induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (Rob.) niessel. Journal of Chemical Ecology 28: 2429-2448.
47. MARAK, H. B., A. BIERE, AND J. M. M. VAN DAMME. 2003. Fitness costs of chemical defense in Plantago lanceolata L.: Effects of nutrient and competition stress. Evolution 57: 2519-2530.
48. MCKEY, D. 1974. Adaptive patterns in alkaloid physiology. American Naturalist 108: 305-320.
49. MCKEY, D. 1979. The distribution of secondary compounds within plants. In G. A. Rosenthal and D. H. Janzen [eds.], Herbivores: their interactions with secondary plant metabolites, 55-133. Academic Press, New York, New York, USA.
50. ORIANS, C. M., C. G. HOCHWENDER, R. S. FRITZ, AND T. SNALL. 2010. Growth and chemical defense in willow seedlings: trade-offs are transient. Oecologia 163: 283-290.
51. POTVIN, C., AND D. A. ROFF. 1993. Distribution-free and robust statistical methods-Viable alternatives to parametric statistics. Ecology 74: 1617-1628.
52. QUINTERO, C., AND M. D. BOWERS. 2012. Changes in plant chemical defenses and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae). Oecologia 168: 471-481.
53. RASMANN, S., AND A. A. A GRAWAL. 2008. In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiology 146: 875-880.
54. RHOADES, D. F. 1979. Evolution of plant chemical defense against herbivores. In G. A. Rosenthal and D. H. Janzen [eds.], Herbivores: their interaction with secondary plant metabolites, 1-55. Academic Press, New York, New York, USA.
55. STAMP, N. 2003. Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78: 23-55.
56. STRAUSS, S. Y., J. A. RUDGERS, J. A. LAU, AND R. E. IRWIN. 2002. Direct and ecological costs of resistance to herbivory. Trends in Ecology & Evolution 17: 278-285.
57. THROOP, H. L. 2005. Nitrogen deposition and herbivory affect biomass production and allocation in an annual plant. Oikos 111: 91-100.
58. THROOP, H. L., AND M. T. LERDAU. 2004. Effects of nitrogen deposition on insect herbivory: Implications for community and ecosystem processes. Ecosystems 7: 109-133.
59. VAN DAM, N. M. 2009. Belowground herbivory and plant defenses. Annual Review of Ecology, Evolution, and Systematics 40: 373-391.
60. VAN DER PUTTEN, W. H. 2003. Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84: 2269-2280.
61. VAN DER PUTTEN, W. H., L. E. M. VET, J. A. HARVEY, AND F. L. WACKERS. 2001. Linking above-and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology & Evolution 16: 547-554.
62. VITOUSEK, P. M., J. D. ABER, R. W. HOWARTH, G. E. LIKENS, P. A. MATSON, D. W. SCHINDLER, W. H. SCHLESINGER, AND D. G. TILMAN. 1997. Human alteration of the global nitrogen cycle: Sources and consequences. Ecological Applications 7: 737-750.
63. VITOUSEK, P. M., S. PORDER, B. Z. HOULTON, AND O. A. CHADWICK. 2010. Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20: 5-15.
64. VOITSEKHOVSKAJA, O. V., O. A. KOROLEVA, D. R. BATASHEV, C. KNOP, A. D. TOMOS, Y. V. GAMALEI, H.-W. HELDT, AND G. LOHAUS. 2006. Phloem loading in two Scrophulariaceae species. What can drive symplastic fl ow via plasmodesmata? Plant Physiology 140: 383-395.
65. VUJNOVIC, K., AND R. W. WEIN. 1997. The biology of Canadian weeds. 106. Linaria dalmatica (L.) Mill. Canadian Journal of Plant Science 77: 483-491.
66. WILSON, L. M., S. E. SING, R. W. PIPER, R. HANSEN, D. K. DE CLERCK-FLOATE, D. K. MACKINNON, AND C. RANDALL. 2005. Biology and biological control of Dalmatian and yellow toadfl ax. USDA Forest Service, FHTET-05-13.
67. WURST, S., N. M. VAN DAM, F. MONROY, A. BIERE, AND W. H. VAN DER PUTTEN. 2008. Intraspecifi c variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. Journal of Chemical Ecology 34: 1360-1367.
68. ZEHNDER, C. B., AND M. D. HUNTER. 2008. Effects of nitrogen deposition on the interaction between an aphid and its host plant. Ecological Entomology 33: 24-30.