Advertisement

Plant Ecology

, Volume 219, Issue 8, pp 985–997 | Cite as

Floral-induced and constitutive defense against florivory: a comparison of chemical traits in 12 herb species

  • Kae Wakabayashi
  • Michio Oguro
  • Tomoyuki Itagaki
  • Satoki Sakai
Article
  • 91 Downloads

Abstract

Little is known about how plants protect flowers—their reproductive organs—against florivory. Additionally, the induced floral defense system has been examined in only a few species. We tested the inducibility of putative floral defenses and investigated the relationship between natural florivory and the floral defenses of 12 naturally growing plant species. The relationships between florivory and four chemical traits (nitrogen, phosphorus, total phenolics, and condensed tannins) were investigated in 12 plant species. We also studied whether flowers induce changes in chemical defenses in response to artificial damage in 10 plant species. A higher concentration of floral nitrogen was associated with a decreasing frequency of florivore attacks. Among the four traits of the 10 plant species studied, no trait changed in response to the artificial damage. We suggest that induced defense systems may not be advantageous for flowers, although it is also possible that these species simply do not use induced defense in any of their plant parts.

Keywords

Floral defense Floral herbivory Total phenolics Condensed tannins Nitrogen Phosphorus 

Notes

Acknowledgements

The authors thank C. Oka, J. Mochizuki, and K. Hoshi for their help during the fieldwork, as well as S. Takayanagi, R. Oguchi, H. Kurokawa, K. Hashimoto, M. Kawabe, and M. Inoue for their advice regarding the chemical analyses. The authors also thank our colleagues, particularly T. Nakashizuka, K. Hikosaka, M. Maki, and M. Aiba, for their valuable suggestions throughout the study.

Supplementary material

11258_2018_851_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 33 kb)
11258_2018_851_MOESM2_ESM.xlsx (12 kb)
Supplementary material 2 (XLSX 13 kb)

References

  1. Adler LS, Karban R, Strauss SY (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82:2032–2044CrossRefGoogle Scholar
  2. Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutrients increase nectar alkaloids. Ecol Lett 9:960–967CrossRefPubMedGoogle Scholar
  3. Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett 15:1140–1148CrossRefPubMedGoogle Scholar
  4. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949CrossRefGoogle Scholar
  5. Alves MN, Sartoratto A, Trigo JR (2007) Scopolamine in Brugmansia suaveolens (Solanaceae): defense, allocation, costs, and induced response. J Chem Ecol 33:297–309CrossRefPubMedGoogle Scholar
  6. Barbehenn RV, Constabel CP (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565CrossRefPubMedGoogle Scholar
  7. Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633CrossRefGoogle Scholar
  8. Bernays EA, Driver GC, Bilgener M (1989) Herbivores and plant tannins. In: Begon M, Fitter AH, Ford ED, MacFadyen A (eds) Advances in ecological research. Academic Press, Cambridge, pp 263–302Google Scholar
  9. Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330CrossRefPubMedGoogle Scholar
  10. Boyer MDH, Soper Gorden NL, Barber NA, Adler LS (2016) Floral damage induces resistance to florivory in Impatiens capensis. Arthropod-Plant Interact 10:121–131CrossRefGoogle Scholar
  11. Cárdenas RE, Valencia R, Kraft NJB, Argoti A, Dangles O, Swenson N (2014) Plant traits predict inter- and intraspecific variation in susceptibility to herbivory in a hyperdiverse Neotropical rain forest tree community. J Ecol 102:939–952CrossRefGoogle Scholar
  12. Chen M-S (2008) Inducible direct plant defense against insect herbivores: A review. Insect Sci 15:101–114CrossRefGoogle Scholar
  13. Clancy KM, King RM (1993) Defining the western spruce budworm’s nutritional niche with response surface methodology. Ecology 74:442–454CrossRefGoogle Scholar
  14. Coley PD (1987) Interspecific variation in plant anti-herbivore properties: the role of habitat quality and rate of disturbance. New Phytol 106:251–263CrossRefGoogle Scholar
  15. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899CrossRefPubMedGoogle Scholar
  16. De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CMJ (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363CrossRefPubMedPubMedCentralGoogle Scholar
  17. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry. Bioscience 46:674–684CrossRefGoogle Scholar
  18. Euler M, Baldwin IT (1996) The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107:102–112CrossRefPubMedGoogle Scholar
  19. Farre-Armengol G, Filella I, Llusia J, Primante C, Penuelas J (2015) Enhanced emissions of floral volatiles by Diplotaxis erucoides (L.) in response to folivory and florivory by Pieris brassicae (L.). Biochem Syst Ecol 63:51–58CrossRefGoogle Scholar
  20. Feeny P (1975) Biochemical coevolution between plants and their insect herbivores. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 3–19Google Scholar
  21. Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Recent advances in phytochemistry, vol 10. Plenum Press, New York, pp 1–40Google Scholar
  22. Fleming PA, Hofmeyr SD, Nicolson SW, du Toit JT (2006) Are giraffes pollinators or flower predators of Acacia nigrescens in Kruger National Park, South Africa? J Trop Ecol 22:247–253CrossRefGoogle Scholar
  23. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  24. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage Publishing, Thousand OaksGoogle Scholar
  25. Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243CrossRefPubMedGoogle Scholar
  27. Helms AM, De Moraes CM, Troger A, Alborn HT, Francke W, Tooker JF, Mescher MC (2017) Identification of an insect-produced olfactory cue that primes plant defenses. Nat Commun 8:9CrossRefGoogle Scholar
  28. Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 62:2465–2483CrossRefPubMedGoogle Scholar
  29. Howe G, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  30. Huang W, Siemann E, Yang X, Wheeler GS, Ding J (2013) Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores. Proc R Soc B 280:20131318CrossRefPubMedGoogle Scholar
  31. Irwin RE, Adler LS (2006) Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant. Am J Bot 93:64–72CrossRefGoogle Scholar
  32. Ishizaki S, Shiojiri K, Karban R, Ohara M (2016) Seasonal variation of responses to herbivory and volatile communication in sagebrush (Artemisia tridentata) (Asteraceae). J Plant Res 129:659–666CrossRefPubMedGoogle Scholar
  33. Istatkova R, Tashev A, Popova P, Philipov S (2011) Alkaloid composition of Thalictrum minus L. subsp. minus (Ranunculaceae Juss.). Comptes Rendus De L Academie Bulgare Des Sciences 64:1109–1116Google Scholar
  34. Johnson E, Berhow M, Dowd P (2008) Colored and white sectors from star-patterned petunia flowers display differential resistance to corn earworm and cabbage looper larvae. J Chem Ecol 34:757–765CrossRefPubMedGoogle Scholar
  35. Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows—methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217CrossRefGoogle Scholar
  36. Kaczorowski RL, Koplovich A, Sporer F, Wink M, Markman S (2014) Immediate effects of nectar robbing by palestine sunbirds (Nectarinia osea) on nectar alkaloid concentrations in tree tobacco (Nicotiana glauca). J Chem Ecol 40:325–330CrossRefPubMedGoogle Scholar
  37. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  38. Karban R, Myers JH (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20:297–330CrossRefGoogle Scholar
  39. Karban R, Agrawa AA, Thaler JS, Adler LS (1999) Induced plant responses and information content about risk of herbivory. Trends Ecol Evol 14:443–447CrossRefPubMedGoogle Scholar
  40. Kessler A, Halitschke R (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct Ecol 23:901–912CrossRefGoogle Scholar
  41. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202CrossRefPubMedGoogle Scholar
  42. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–1780CrossRefPubMedGoogle Scholar
  43. Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149CrossRefGoogle Scholar
  44. Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280CrossRefPubMedGoogle Scholar
  45. Li YK, Zhao QJ, Hu J, Zou Z, He XY, Yuan HB, Shi XY (2009) Two new quinoline alkaloid mannopyranosides from Solidago canadensis. Helv Chim Acta 92:928–931CrossRefGoogle Scholar
  46. Liu PY, Liu D, Li WH, Zhao T, Sauriol F, Gu YC, Shi QW, Zhang ML (2015) Chemical constituents of plants from the genus Eupatorium (1904–2014). Chem Biodivers 12:1481–1515CrossRefPubMedGoogle Scholar
  47. Lucas-Barbosa D, van Loon JJA, Dicke M (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–1654CrossRefPubMedGoogle Scholar
  48. Lucas-Barbosa D, Sun P, Hakman A, van Beek T, van Loon J, Dicke M (2016) Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Funct Ecol 30:431–441CrossRefGoogle Scholar
  49. Makkar HPS, Gamble G, Becker K (1999) Limitation of the butanol–hydrochloric acid–iron assay for bound condensed tannins. Food Chem 66:129–133CrossRefGoogle Scholar
  50. Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  51. McArt S, Halitschke R, Salminen J, Thaler J (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology 94:966–975CrossRefGoogle Scholar
  52. McCall AC (2006) Natural and artificial floral damage induces resistance in Nemophila menziesii (Hydrophyllaceae) flowers. Oikos 112:660–666CrossRefGoogle Scholar
  53. McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98:985–992CrossRefGoogle Scholar
  54. McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365CrossRefPubMedGoogle Scholar
  55. McCall AC, Karban R (2006) Induced defense in Nicotiana attenuata (Solanaceae) fruit and flowers. Oecologia 146:566–571CrossRefPubMedGoogle Scholar
  56. McCall A, Murphy S, Venner C, Brown M (2013) Florivores prefer white versus pink petal color morphs in wild radish, Raphanus sativus. Oecologia 172:189–195CrossRefPubMedGoogle Scholar
  57. McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320CrossRefGoogle Scholar
  58. Moreira X, Abdala-Roberts L, Hernández-Cumplido J, Cuny MAC, Glauser G, Benrey B (2015) Specificity of induced defenses, growth, and reproduction in lima bean (Phaseolus lunatus) in response to multispecies herbivory. Am J Bot 102:1300–1308CrossRefPubMedGoogle Scholar
  59. Oguro M, Sakai S (2014) Difference in defense strategy in flower heads and leaves of Asteraceae: multiple-species approach. Oecologia 174:227–239CrossRefPubMedGoogle Scholar
  60. Oguro M, Sakai S (2015) Relation between flower head traits and florivory in Asteraceae: a phylogenetically controlled approach. Am J Bot 102:407–416CrossRefPubMedGoogle Scholar
  61. Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 81:1765–1783CrossRefGoogle Scholar
  62. Onodera H, Oguro M, Sakai S (2014) Effects of nutrient contents and defense compounds on herbivory in reproductive organs and leaves of Iris gracilipes. Plant Ecol.  https://doi.org/10.1007/s11258-014-0359-2 Google Scholar
  63. Pan Y, Zhao YL, Zhang J, Li WY, Wang YZ (2016) Phytochemistry and pharmacological activities of the genus Gentiana (Gentianaceae). Chem Biodivers 13:107–150CrossRefPubMedGoogle Scholar
  64. Perkins MC, Woods HA, Harrison JF, Elser JJ (2004) Dietary phosphorus affects the growth of larval Manduca sexta. Arch Insect Biochem Physiol 55:153–168CrossRefPubMedGoogle Scholar
  65. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  66. Reese JC, Chan BG, Waiss AC (1982) Effects of cotton condensed tannin, maysin (corn) and pinitol (soybeans) on Heliothis zea growth and development. J Chem Ecol 8:1429–1436CrossRefPubMedGoogle Scholar
  67. Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 1–55Google Scholar
  68. Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. In: Wallace JW, Mansell RL (eds) Recent advances in phytochemistry, vol 10. Plenum Press, New York, pp 168–213Google Scholar
  69. Salminen J-P, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338CrossRefGoogle Scholar
  70. Sashida Y, Ori K, Mimaki Y (1991) Studies on the chemical constituents of the bulbs of Lilium mackliniae. Chem Pharm Bull 39:2362–2368CrossRefGoogle Scholar
  71. Sharma DK, Gupta V, Mondal D, Singh M, Mandal R, Raguvaran R (2015) Evaluation of in vitro antioxidant capacity of aqueous and ethanolic extracts of eight different plants materials. Int J Pharm Sci Res 6:4086Google Scholar
  72. Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2016) Generalized linear mixed models using ‘AD Model Builder’Google Scholar
  73. Smilanich AM, Fincher RM, Dyer LA (2016) Does plant apparency matter? Thirty years of data provide limited support but reveal clear patterns of the effects of plant chemistry on herbivores. New Phytol 210:1044–1057CrossRefPubMedGoogle Scholar
  74. Soper Gorden NL, Adler LS (2016) Florivory shapes both leaf and floral interactions. Ecosphere 7:e01326CrossRefGoogle Scholar
  75. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Quart Rev Biol 78:23–55CrossRefPubMedGoogle Scholar
  76. Sterner RW, Elser JJ (2002) Imbalanced resources and animal growth. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, pp 179–230Google Scholar
  77. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285CrossRefGoogle Scholar
  78. 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 92:132–141CrossRefGoogle Scholar
  79. Tao L, Hunter MD (2013) Allocation of resources away from sites of herbivory under simultaneous attack by aboveground and belowground herbivores in the common milkweed, Asclepias syriaca. Arthropod-Plant Interact 7:217–224CrossRefGoogle Scholar
  80. Tsuji K, Sota T (2010) Sexual differences in flower defense and correlated male-biased florivory in a plant–florivore system. Oikos 119:1848–1853CrossRefGoogle Scholar
  81. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253CrossRefPubMedGoogle Scholar
  82. Wang Y-H, Gao S, Yang F-M, Sun Q-Y, Wang J-S, Liu H-Y, Li C-S, Di Y-T, Li S-L, He H-P, Hao X-J (2007) Structure elucidation and biomimetic synthesis of hostasinine A, a new benzylphenethylamine alkaloid from Hosta plantaginea. Org Lett 9:5279–5281CrossRefPubMedGoogle Scholar
  83. Wetzel RG, Likens GE (2000) Limnological analyses. Springer, New YorkCrossRefGoogle Scholar
  84. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefPubMedGoogle Scholar
  85. Yamashita H, Takeda K, Haraguchi M, Abe Y, Kuwahara N, Suzuki S, Terui A, Masaka T, Munakata N, Uchida M, Nunokawa M, Kaneda K, Goto M, Lee K-H, Wada K (2018) Four new diterpenoid alkaloids from Aconitum japonicum subsp. subcuneatum. J Nat Med 72:230–237CrossRefPubMedGoogle Scholar
  86. Zangerl AR, Berenbaum MR (1993) Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47–54CrossRefGoogle Scholar
  87. Zhou S, Lou Y-R, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–1498PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.Forestry and Forest Products Research InstituteTsukubaJapan

Personalised recommendations