Arthropod-Plant Interactions

, Volume 5, Issue 2, pp 125–139

A quantitative evaluation of major plant defense hypotheses, nature versus nurture, and chemistry versus ants

  • Tara Joy Massad
  • R. Malia Fincher
  • Angela M. Smilanich
  • Lee Dyer
Original Paper

Abstract

Variation in plant secondary metabolite content can arise due to environmental and genetic variables. Because these metabolites are important in modifying a plant’s interaction with the environment, many studies have examined patterns of variation in plant secondary metabolites. Investigations of chemical defenses are often linked to questions about the efficacies of plant defenses and hypotheses on their evolution in different plant guilds. We performed a series of meta-analyses to examine the importance of environmental and genetic sources of variation in secondary metabolites as well as the antiherbivore properties of different classes of defense. We found both environmental and genetic variation affect secondary metabolite production, supporting continued study of the carbon-nutrient balance and growth-differentiation balance hypotheses. Defenses in woody plants are more affected by genetic variation, and herbaceous plant defenses are more influenced by environmental variation. Plant defenses in agricultural and natural systems show similar responses to manipulations, as do plants in laboratory, greenhouse, or field studies. What does such variation mean to herbivores? A comparison of biotic, physical, and chemical defenses revealed the most effective defensive strategy for a plant is biotic mutualisms with ants. Fast-growing plants are most often defended with qualitative defenses and slow-growing plants with quantitative defenses, as the plant apparency and resource availability hypotheses predict. However, we found the resource availability hypothesis provides the best explanation for the evolution of plant defenses, but the fact that there is considerable genetic and environmental variation in defenses indicates herbivores can affect plant chemistry in ecological and evolutionary time.

Keywords

Herbivory Generalist Genetic variation Phenotype Plant defense Secondary metabolites Specialist 

Supplementary material

11829_2011_9121_MOESM1_ESM.docx (55 kb)
Supplementary material 1 (DOCX 54 kb)

References

  1. Abrahamson WG, Anderson SS, McCrea KD (1988) Effects of manipulation of plant carbon/nutrient balance on tall goldenrod resistance to a gall making herbivore. Oecologia 77:302–306CrossRefGoogle Scholar
  2. Agrawal AA, Kurashige NS (2003) A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol 29:1403–1415PubMedCrossRefGoogle Scholar
  3. Arany AM, de Jong TJ, Kim HK, van Dam NM, Choi YH, van Mil HGJ, Verpoorte R, van der Meijden E (2009) Genotype-environment interactions affect flower and fruit herbivory and plant chemistry of Arabidopsis thaliana in a transplant experiment. Ecol Resear 24:1161–1171CrossRefGoogle Scholar
  4. Arimura G-I, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515PubMedCrossRefGoogle Scholar
  5. Ayres MP, Clausen TP, MacLean SF Jr, Redman AM, Reichardt PB (1997) Diversity of structure and ant herbivore activity in condensed tannins. Ecology 78:1696–1712CrossRefGoogle Scholar
  6. Baldwin IT, Schultz JC (1983) Rapid changes in leaf chemistry induced by damage: Evidence for communication between plants. Science 221:277PubMedCrossRefGoogle Scholar
  7. Bassman JH (2004) Ecosystem consequences of enhanced solar ultraviolet radiation: Secondary plant metabolites as mediators of multiple trophic interactions in terrestrial plant communities. Photochem Photobiol 79:382–398PubMedCrossRefGoogle Scholar
  8. Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: Nutrients and secondary metabolites. Ecology 83:2489–2501CrossRefGoogle Scholar
  9. Berenbaum M (1983) Coumarins and caterpillars: a case for coevolution. Evolution 37:163–179CrossRefGoogle Scholar
  10. Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New YorkGoogle Scholar
  11. Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892CrossRefGoogle Scholar
  12. Bernays EA, Copper Driver G, Bilgener M (1989a) Herbivores and plant tannins. In: Begon M, Fitter AH, Ford ED, MacFadyen A (eds) Advances in ecological research, vol 19. Academic Press Ltd., New York, pp 263–302Google Scholar
  13. Bernays EA, Cooper Driver G, Bilgener M (1989b) Herbivores and plant tannins. Adv Ecol Res 19:263–302CrossRefGoogle Scholar
  14. Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368CrossRefGoogle Scholar
  15. Bryant JP, Chapin FS III, Reichardt PB, Clausen TP (1987) Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance. Oecologia 72:510–514CrossRefGoogle Scholar
  16. Calcagno MP, Coll J, Lloria J, Faini F, Alonso-Amelot ME (2002) Evaluation of synergism in the feeding deterrence of some furanocoumarins on Spodoptera littoralis. J ChemEcol 28:175–191Google Scholar
  17. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. P Natl Acad Sci USA 100:14555–14561CrossRefGoogle Scholar
  18. Clancy KM, Price PW (1987) Herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68:733–737CrossRefGoogle Scholar
  19. Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–229CrossRefGoogle Scholar
  20. Coley PD (1987) Interspecific variation in plant anti-herbivore properties—the role of habitat quality and rate of disturbance. New Phytol 106S:251–263Google Scholar
  21. Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  22. Cooper H, Hedges LV, Valentine JC (2009) The handbook of research synthesis and meta-analysis, 2nd edn. Russel Sage Foundation Publications, New YorkGoogle Scholar
  23. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522PubMedCrossRefGoogle Scholar
  24. Croteau R, Kutchan TM, Lewis NG (2000) Natural Products. In: Buchanan B, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, USA, pp 1250–1318Google Scholar
  25. Dirr MA (1998) Manual of woody landscape plants: their identification, ornamental characteristics, culture, propagation and uses. Stipes Publishing L.L.C., Champaigne, ILGoogle Scholar
  26. Dobler S, Rowell-Rahier M (1994) Response of a leaf beetle to two food plants, only one of which provides a sequestrable defensive chemical. Oecologia 97:271–277CrossRefGoogle Scholar
  27. Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739PubMedCrossRefGoogle Scholar
  28. Dyer LA (1995) Tasty generalists and nasty specialists? Antipredator mechanisms in tropical Lepidopteran larvae. Ecology 76:1483–1496CrossRefGoogle Scholar
  29. Dyer LA, Dodson CD, Beihoffer J, Letourneau DK (2001) Trade offs in anti-herbivore defenses in Piper cenocladum: ant mutualists versus plant secondary metabolites. J Chem Ecol 27:581–592PubMedCrossRefGoogle Scholar
  30. Dyer LA, Dodson CD, Stireman JO III, Tobler MA, Smilanich AM, Fincher RM, Letourneau DK (2003) Synergistic effects of three Piper amides on generalist and specialist herbivores. J Chem Ecol 29:2499–2514PubMedCrossRefGoogle Scholar
  31. Dyer LA, Dodson CD, Letourneau DK, Tobler MA, Hsu A, Stireman JO III (2004) Ecological causes and consequences of variation in defensive chemistry of a neotropical shrub. Ecology 276:2795–2803CrossRefGoogle Scholar
  32. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  33. Engler-Chaouat HS, Gilber LE (2007) De novo synthesis vs. sequestration: negatively correlated metabolic traits and the evolution of host plant specialization in cyanogenic butterflies. J Chem Ecol 33:25–42PubMedCrossRefGoogle Scholar
  34. Farmer EE (2001) Surface-to-air signals. Nature 411:854–856PubMedCrossRefGoogle Scholar
  35. Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interactions between plants and insects. Plenum, New York, pp 1–40Google Scholar
  36. Green PWC, Stevenson PC, Simmonds MSJ, Sharma HC (2003) Phenolic compounds on the pod-surface of pigeonpea, Cajanus cajan, mediate feeding behavior of Helicoverpa armigera Larvae. J Chem Ecol 29:811–821PubMedCrossRefGoogle Scholar
  37. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  38. Gurevitch J, Hedges LV (2001) Meta analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 347–369Google Scholar
  39. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95CrossRefGoogle Scholar
  40. Harborne JB (1993) Introduction to ecological biochemistry, 4th edn. Academic Press, New YorkGoogle Scholar
  41. Hartmann T, Theuring C, Beuerle T, Ernst L, Singer MS, Bernays EA (2004) Acquired and partially de novo synthesized pyrrolizidine alkaloids in two polyphagous Arctiids and the alkaloid profiles of their larval food-plants. J Chem Ecol 30:229–254PubMedCrossRefGoogle Scholar
  42. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453CrossRefGoogle Scholar
  43. Heil M, Delsinne T, Hilpert A, Schurkens S, Andary C, Linsenmair KE, Sousa SM, McKey D (2002) Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis. Oikos 99:457–468CrossRefGoogle Scholar
  44. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Bio 67:283CrossRefGoogle Scholar
  45. Huang XP, Renwick JAA (1995) Chemical and experiential basis for rejection of Tropaeolum majus by Pieris rapae larvae. J Chem Ecol 21:1601–1617CrossRefGoogle Scholar
  46. Ivey CT, Carr DE, Eubanks MD (2009) Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus. Heredity 102:303–311PubMedCrossRefGoogle Scholar
  47. Janzen DH (1974) Tropical black water rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103CrossRefGoogle Scholar
  48. Jones DG (1998) Piperonyl butoxide: the insect synergist. Academic Press, LondonGoogle Scholar
  49. Karban R (1992) Plant variation: Its effects on populations of herbivorous insects. In: Fritz RS, Sims EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Illinois, pp 195–215Google Scholar
  50. Karban R (2001) Communication between sagebrush and wild tobacco in the field. Biochem Syst Ecol 29:995–1005CrossRefGoogle Scholar
  51. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  52. Keinanen M, Julkunen-Tiitto R, Mutikainen P, Walls M, Ovaska J, Vapaavuori E (1999) Trade-offs in phenolic metabolism of silver birch: effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986Google Scholar
  53. Kindscher K, Wells PV (1995) Prairie plant guilds: a multivariate analysis of prairie species based on ecological and morphological traits. Vegetatio 117:29–50CrossRefGoogle Scholar
  54. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant ant herbivore defenses. Ecology 83:176–190CrossRefGoogle Scholar
  55. Koricheva J, Larsson S, Haukioja E, Keinanen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of metaanalysis. Oikos 83:212–226CrossRefGoogle Scholar
  56. Koricheva J, Nykanen H, Gianoli E (2004) Meta-analysis of trade-offs among plant anitherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75PubMedCrossRefGoogle Scholar
  57. Lambers H, Chapin FS III, Pons TL (1998) Plant physiological ecology. Springer, New YorkGoogle Scholar
  58. Lerdau M, Coley PD (2002) Benefits of the carbon-nutrient balance hypothesis. Oikos 98:534–536CrossRefGoogle Scholar
  59. Lill JT, Marquis RJ (2001) The effects of leaf quality on herbivore performance attack from natural enemies. Oecoloiga 126:418–428CrossRefGoogle Scholar
  60. Lindroth RL (1988) Adaptations of mammalian herbivores to plant chemical defenses. In: Spencer KC (ed) Chemical mediation of coevolution. Academic Press, New York, NY, pp 415–445Google Scholar
  61. Marquis RJ (1992) Selective impact of herbivores. In: Fritz RS, Sims EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Illinois, pp 301–325Google Scholar
  62. Martin JS, Martin MM, Bernays EA (1987) Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: Implications for theories of plant defense. J Chem Ecol 13:605–621CrossRefGoogle Scholar
  63. Massad TJ, Dyer LA (2010) A meta-analysis of the effects of global environmental change on plant-herbivore interactions. Arthropod-Plant Interactions 4:181–188CrossRefGoogle Scholar
  64. Montllor CB, Bernays EA, Barbehenn RV (1990) Importance of quinolizindine alkaloids in the relationship between larvae of Uresiphita reversalis (Lepidoptera: Pyralidae) and a host plant, Genista monspessulana. J Chem Ecol 16:1853–1856CrossRefGoogle Scholar
  65. Nelson AC, Kursar TA (1999) Interactions among plant defense compounds: a method for analysis. Chemoecology 2:81–92CrossRefGoogle Scholar
  66. Nichols-Orians CM (1991) Environmentally induced differences in plant traits: consequences for susceptibility to a leaf-cutter ant. Ecology 72:1609–1623CrossRefGoogle Scholar
  67. Nykanen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268CrossRefGoogle Scholar
  68. Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459PubMedCrossRefGoogle Scholar
  69. Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303PubMedCrossRefGoogle Scholar
  70. Palumbo MJ, Putz FE, Talcott ST (2007) Nitrogen fertilizer and gender effects on the secondary metabolism of yaupon, a caffeine-containing North American holly. Oecologia 151:1–9PubMedCrossRefGoogle Scholar
  71. Price PW (1997) Insect ecology, 3rd edn. Wiley, New YorkGoogle Scholar
  72. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  73. Rendina-Gobioff G, Kromrey JD (2006) PUB_BIAS: a SAS macro for detecting publication bias in meta-analysis. http://analytics.ncsu.edu/sesug/2006/PO04_06.PDF
  74. Rhoades DF (1979) Evolution of plant chemical defenses against herbivory. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54Google Scholar
  75. Rhoades DF, Cates RG (1976) Toward a general theory of plant antiherbivore chemistry. In: Wallace J, Mansell R (eds) Biochemical interactions between plants and insects. Recent advances in phytochemistry, vol 10. Plenum Press, New York, pp 168–213Google Scholar
  76. Romeo JT, Saunders JA, Barbosa P (1996) Phytochemical diversity and redundancy in ecological interactions. recent advances in phytochemistry, vol 30. Plenum Press, New YorkGoogle Scholar
  77. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464–468PubMedGoogle Scholar
  78. Rosenthal GA, Berenbaum M (1991) Herbivores, their interaction with secondary plant metabolites. Academic Press, New YorkGoogle Scholar
  79. Rosumek FB, Silveira FAO, de Neves SF, de Barbosa NPU, Diniz L, Oki Y, Pezzini F, Fernandez GW, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549PubMedCrossRefGoogle Scholar
  80. Silvertown J, Dodd M (1996) Comparing plants and connecting traits. Philos T Roy Soc B 351:1233–1239CrossRefGoogle Scholar
  81. Singer MS, Stireman JO (2005) The tri-trophic niche concept and adaptive radiation of phytophagous insects. Ecol Let 8:1247–1255CrossRefGoogle Scholar
  82. Smilanich AM (2008) Variation in plant chemical defense and the physiological response of specialist and generalist herbivores. Dissertation, Tulane UniversityGoogle Scholar
  83. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55PubMedCrossRefGoogle Scholar
  84. Stermitz FR, Lorenz P, Tawara JN, Zenewicz LA, Lewis K (2000) Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5′-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci USA 97:1433–1437PubMedCrossRefGoogle Scholar
  85. Theodoratus DH, Bowers MD (1999) Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider, Lycosa carolinensis. J Chem Ecol 25:283–295CrossRefGoogle Scholar
  86. Tuomi J, Niemala P, Chapin FSI, Bryant JP, Siren S (1988) Defensive responses of trees in relation to their carbon/nutrient balance. In: Mattson WJ (ed) Mechanisms of woody plant defenses against insects: search for pattern. Springer, New York, pp 57–72Google Scholar
  87. Williamson EM (2001) Synergy and other interactions in phytomedicines. Phytomedicine 8:401–409PubMedCrossRefGoogle Scholar
  88. Zalucki MP, Malcolm SB (1999) Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. J Chem Ecol 25:1827–1842CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Tara Joy Massad
    • 1
    • 2
  • R. Malia Fincher
    • 3
  • Angela M. Smilanich
    • 4
  • Lee Dyer
    • 4
  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.Max Planck Institute of BiogeochemistryJenaGermany
  3. 3.Department of BiologySamford UniversityBirminghamUSA
  4. 4.Department of BiologyUniversity of NevadaRenoUSA

Personalised recommendations