, Volume 176, Issue 3, pp 811–824 | Cite as

Chemical defense lowers plant competitiveness

  • Daniel J. Ballhorn
  • Adrienne L. Godschalx
  • Savannah M. Smart
  • Stefanie Kautz
  • Martin Schädler
Plant-microbe-animal interactions - Original research


Both plant competition and plant defense affect biodiversity and food web dynamics and are central themes in ecology research. The evolutionary pressures determining plant allocation toward defense or competition are not well understood. According to the growth–differentiation balance hypothesis (GDB), the relative importance of herbivory and competition have led to the evolution of plant allocation patterns, with herbivore pressure leading to increased differentiated tissues (defensive traits), and competition pressure leading to resource investment towards cellular division and elongation (growth-related traits). Here, we tested the GDB hypothesis by assessing the competitive response of lima bean (Phaseolus lunatus) plants with quantitatively different levels of cyanogenesis—a constitutive direct, nitrogen-based defense against herbivores. We used high (HC) and low cyanogenic (LC) genotypes in different competition treatments (intra-genotypic, inter-genotypic, interspecific), and in the presence or absence of insect herbivores (Mexican bean beetle, Epilachna varivestis) to quantify vegetative and generative plant parameters (above and belowground biomass as well as seed production). Highly defended HC-plants had significantly lower aboveground biomass and seed production than LC-plants when grown in the absence of herbivores implying significant intrinsic costs of plant cyanogenesis. However, the reduced performance of HC- compared to LC-plants was mitigated in the presence of herbivores. The two plant genotypes exhibited fundamentally different responses to various stresses (competition, herbivory). Our study supports the GDB hypothesis by demonstrating that competition and herbivory affect different plant genotypes differentially and contributes to understanding the causes of variation in defense within a single plant species.


Cyanogenesis Herbivory Growth-differentiation balance hypothesis Lima bean Tradeoff 



Startup funds to D.J.B. from Portland State University are gratefully acknowledged. S.K. was supported by a postdoctoral fellowship (grant LPDS 2009-29) from the German Academy of Sciences Leopoldina. The authors declare that they have no conflict of interest.


  1. Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett 15:1140–1148. doi: 10.1111/j.1461-0248.2012.01838.x PubMedCrossRefGoogle Scholar
  2. Agrawal AA (2007) Macroevolution of plant defense strategies. Trends Ecol Evol 22:103–109. doi: 10.1016/j.tree.2006.10.012 PubMedCrossRefGoogle Scholar
  3. Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432. doi: 10.1111/j.1365-2435.2010.01796.x CrossRefGoogle Scholar
  4. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149PubMedCrossRefGoogle Scholar
  5. Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. In: Bell MA, Eanes WF, Futuyma DJ, Levinton JS (eds) Evolution after Darwin: the first 150 years. Sinauer, SunderlandGoogle Scholar
  6. Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science (80-) 193:24–29CrossRefGoogle Scholar
  7. Baldwin IT, Hamilton W (2000) Jasmonate-induced responses of Nicotiana sylvestris results in fitness costs due to impaired competitve ability for nitrogen. J Chem Ecol 26:915–952CrossRefGoogle Scholar
  8. Baldwin IT, Sims CL, Kean SE (1990) The reproductive consequences associated with inducible alkaloidal responses in wild tobacco. Ecology 71:252–262CrossRefGoogle Scholar
  9. Ballhorn DJ (2011a) Cyanogenic glycosides in nuts and seeds. In: Preedy VR, Watson RR, Patel VB (eds) Nuts and seeds health and disease prevention (1st edn). Elsevier, Amsterdam, pp 129–136CrossRefGoogle Scholar
  10. Ballhorn DJ (2011b) Constraints of simultaneous resistance to a fungal pathogen and an insect herbivore in lima bean (Phaseolus lunatus L.). J Chem Ecol 37:141–144. doi: 10.1007/s10886-010-9905-0 PubMedCrossRefGoogle Scholar
  11. Ballhorn DJ, Lieberei R, Ganzhorn JU (2005) Plant cyanogenesis of Phaseolus lunatus and its relevance for herbivore–plant interaction: the importance of quantitative data. J Chem Ecol 31:1445–1473. doi: 10.1007/s10886-005-5791-2 PubMedCrossRefGoogle Scholar
  12. Ballhorn DJ, Heil M, Pietrowski A, Lieberei R (2007) Quantitative effects of cyanogenesis on an adapted herbivore. J Chem Ecol 33:2195–2208. doi: 10.1007/s10886-007-9380-4 PubMedCrossRefGoogle Scholar
  13. Ballhorn DJ, Kautz S, Lion U, Heil M (2008a) Quantitative variability of lima bean’s VOC boquets and its putative ecological consequences. Plant Signal Behav 3:1005–1007. doi: 10.1111/j.1365-2745.2008.01404.x. www.landesbioscience.com PubMedPubMedCentralGoogle Scholar
  14. Ballhorn DJ, Kautz S, Lion U, Heil M (2008b) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971–980. doi: 10.1111/j.1365-2745.2008.01404.x CrossRefGoogle Scholar
  15. Ballhorn DJ, Kautz S, Heil M, Hegeman AD (2009) Cyanogenesis of wild lima bean (Phaseolus lunatus L.) is an efficient and direct defense in nature. PLoS ONE e5450Google Scholar
  16. Ballhorn DJ, Pietrowski A, Lieberei R (2010) Direct trade-off between cyanogenesis and resistance to a fungal pathogen in lima bean (Phaseolus lunatus L.). J Ecol 98:226–236. doi: 10.1111/j.1365-2745.2009.01591.x CrossRefGoogle Scholar
  17. Ballhorn DJ, Kautz S, Jensen M, Schmitt I, Heil M, Hegeman AD (2011a) Genetic and environmental interactions determine plant defences against herbivores. J Ecol 99:313–326. doi: 10.1111/j.1365-2745.2010.01747.x CrossRefGoogle Scholar
  18. Ballhorn DJ, Schmitt I, Fankhauser JD, Katagiri F, Pfanz H (2011b) CO2-mediated changes of plant traits and their effects on herbivores are determined by leaf age. Ecol Entomol 36:1–13. doi: 10.1111/j.1365-2311.2010.01240.x CrossRefGoogle Scholar
  19. Ballhorn DJ, Godschalx AL, Kautz S (2013a) Co-variation of chemical and mechanical defenses in lima bean (Phaseolus lunatus L.). J Chem Ecol 39:413–417. doi: 10.1007/s10886-013-0255-6 PubMedCrossRefGoogle Scholar
  20. Ballhorn DJ, Kautz S, Heil M (2013b) Distance and sex determine host plant choice by herbivorous beetles. PLoS ONE 8(2):e55602Google Scholar
  21. Ballhorn DJ, Kautz S, Schädler M (2013c) Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172:833–846Google Scholar
  22. Ballhorn DJ, Kay J, Kautz S (2014) Quantitative effects of leaf area removal on indirect defense of lima bean (Phaseolus lunatus) in nature. J Chem Ecol (in press)Google Scholar
  23. Barton KE (2007) Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. Am J Bot 94:56–66. doi: 10.3732/ajb.94.1.56 PubMedCrossRefGoogle Scholar
  24. Bennett AE, Bever JD, Deane Bowers M (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:771–779. doi: 10.1007/s00442-009-1338-5 PubMedCrossRefGoogle Scholar
  25. Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892CrossRefGoogle Scholar
  26. Bixenmann RJ, Coley PD, Kursar TA (2013) Developmental changes in direct and indirect defenses in the young leaves of the neotropical tree genus Inga (Fabaceae). Biotropica 45:175–184CrossRefGoogle Scholar
  27. Broz AK, Broeckling CD, De-la-Peña C et al (2010) Plant neighbor identity influences plant biochemistry and physiology related to defense. BMC Plant Biol 10:1–14CrossRefGoogle Scholar
  28. Campbell SA, Kessler A (2013) Plant mating system transitions drive the macroevolution of defense strategies. Proc Natl Acad Sci USA 110:3973–3978. doi: 10.1073/pnas.1213867110 PubMedCrossRefPubMedCentralGoogle Scholar
  29. Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570CrossRefGoogle Scholar
  30. Caswell H (1989) Matrix population models, 2nd edn. Sinauer, SunderlandGoogle Scholar
  31. Chase JM, Abrams PA, Grover JP et al (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315. doi: 10.1046/j.1461-0248.2002.00315.x CrossRefGoogle Scholar
  32. Cipollini D, Heil M (2010) Costs and benefits of induced resistance to herbivores and pathogens in plants. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 5:1–25. doi: 10.1079/PAVSNNR20105005 Google Scholar
  33. Connell JH (1983) On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am Soc Nat 122:661–696CrossRefGoogle Scholar
  34. Cork SJ (1996) Optimal digestive strategies for arboreal herbivorous mammals in contrasting forest types: why koalas and colobines are different. Aust J Ecol 21:10–20Google Scholar
  35. Dantas VDL, Batalha MA (2012) Can antiherbivory resistance explain the abundance of woody species in a Neotropical savanna? Botany 90:93–99. doi: 10.1139/B11-087 CrossRefGoogle Scholar
  36. Dover BA, Noblet R, Moore RF, Culbertson D (1988) An improved artificial diet for Mexican bean beetles based on host preference. J Agric Entomol 5:79–86Google Scholar
  37. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution (NY) 18:586–608CrossRefGoogle Scholar
  38. Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Flanders RV (1984) Comparisons of bean varieties currently being used to culture the Mexican bean beetle (Coleoptera: Coccinellidae). Environ Entomol 13:995–999Google Scholar
  40. Frehner M, Conn EE (1987) The linamarin beta-glucosidase in Costa Rican wild lima beans (Phaseolus lunatus L.) is apoplastic. Plant Physiol 84:1296–1300PubMedCrossRefPubMedCentralGoogle Scholar
  41. García MB, Ehrlén J (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. Am J Bot 89:1295–1302. doi: 10.3732/ajb.89.8.1295 PubMedCrossRefGoogle Scholar
  42. Haag JJ, Coupe MD, Cahill JFJ (2004) Antagonistic interactions between competition and insect herbivory on plant growth. J Ecol 92:156–167CrossRefGoogle Scholar
  43. Hayden KJ, Parker IM (2002) Plasticity in cyanogenesis of Trifolium repens L.: inducibility, fitness costs and variable expression. Evol Ecol Res 4:155–168Google Scholar
  44. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156CrossRefGoogle Scholar
  45. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  46. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  47. Johnson MTJ (2008) Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89:145–154PubMedCrossRefGoogle Scholar
  48. Jones PR, Møller BL, Høj PB (1999) The UDP-glucose: p-hydroxymandelonitrile-O-glucosyltransferase that catalyzes the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor. J Biol Chem 274:35483–35491PubMedCrossRefGoogle Scholar
  49. Kakes P (1990) Properties and functions of the cyanogenic system in higher plants. Euphytica 48:25–43Google Scholar
  50. Kaplan I, Dively GP, Denno RF (2009) The costs of anti-herbivore defense traits in agricultural crop plants: a case study involving leafhoppers and trichomes. Ecol Appl 19:864–872PubMedCrossRefGoogle Scholar
  51. Kempel A, Schädler M, Chrobock T et al (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci USA 108:5685–5689. doi: 10.1073/pnas.1016508108 PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kost C, Heil M (2008) The defensive role of volatile emission and extrafloral nectar secretion for lima bean in nature. J Chem Ecol 34:1–13. doi: 10.1007/s10886-007-9404-0 PubMedCrossRefGoogle Scholar
  53. LaPidus JB, Cleary RW, Davidson RH et al (1963) Chemical factors influencing host selection by Mexican bean beetle Epilachna varivestis Muls. Agric Food Chem 11:462–463CrossRefGoogle Scholar
  54. Lieberei R (1988) Relationship of cyanogenic capacity (HCN-c) of the rubber tree Hevea brasiliensis to susceptibility to Microcyclus ulei, the agent causing South American leaf blight. J Phytopathol 122:54–67Google Scholar
  55. Marak HB, Biere a, Van Damme JMM (2000) Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J Evol Biol 13:985–996. doi: 10.1046/j.1420-9101.2000.00233.x CrossRefGoogle Scholar
  56. Marak HB, Biere A, Van Damme JMM (2003) Fitness costs of chemical defense in Plantago lanceolata L.: effects of nutrient and competition stress. Evolution 57:2519–2530PubMedCrossRefGoogle Scholar
  57. Massad TJ, Dyer LA, Vega CG (2012) Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense. PLoS ONE 7:e47554. doi: 10.1371/journal.pone.0047554 PubMedCrossRefPubMedCentralGoogle Scholar
  58. Moles AT, Peco B, Wallis IR et al (2013) Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytol 198:252–263. doi: 10.1111/nph.12116 PubMedCrossRefGoogle Scholar
  59. Noitsakis B, Jacquard P (1992) Competition between cyanogenic and acyanogenic morphs of Trifolium repens. Theor Appl Genet 83:443–450PubMedCrossRefGoogle Scholar
  60. Nomura M, Hatada A, Itioka T (2011) Correlation between the leaf turnover rate and anti-herbivore defence strategy (balance between ant and non-ant defences) amongst ten species of Macaranga (Euphorbiaceae). Plant Ecol 212:143–155. doi: 10.1007/s11258-010-9810-1 CrossRefGoogle Scholar
  61. Rask L, Andréasson E, Ekbom B et al (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–113PubMedCrossRefGoogle Scholar
  62. Read J, Sanson GD, Caldwell E et al (2009) Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia. Ann Bot 103:757–767. doi: 10.1093/aob/mcn246 PubMedCrossRefPubMedCentralGoogle Scholar
  63. Rees M (1995) Community structure in sand dune annuals: is seed weight a key quantity? Oecologia 83:857–863Google Scholar
  64. Rees M, Brown VK (1992) Interactions between invertebrate herbivores and plant competition. J Ecol 80:353–360CrossRefGoogle Scholar
  65. Richards AJ, Fletcher A (2002) The effects of altitude, aspect, grazing and time on the proportion of cyanogenics in neighbouring populations of Trifolium repens L. (white clover). Heredity 88:432–436Google Scholar
  66. Selmar D, Lieberei R, Conn EE, Biehl B (1989) a -Hydroxynitrile lyase inHevea brasiliensis and its significance for rapid cyanogenesis. Physiol Plant 75: 97–101Google Scholar
  67. Schädler M, Brandl R, Haase J (2007) Antagonistic interactions between plant competition and insect herbivory. J Ecol 88:1490–1498CrossRefGoogle Scholar
  68. Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83:505–517CrossRefGoogle Scholar
  69. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr Comp Biol 42:369–380Google Scholar
  70. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55PubMedCrossRefGoogle Scholar
  71. Thamer S, Schädler M, Bonte D, Ballhorn DJ (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209–219. doi: 10.1007/s11104-010-0635-4 CrossRefGoogle Scholar
  72. Viola DV, Mordecai EA, Jaramillo AG et al (2010) Competition-defense tradeoffs and the maintenance of plant diversity. Proc Natl Acad Sci USA 107:17217–17222. doi: 10.1073/pnas.1007745107 PubMedCrossRefPubMedCentralGoogle Scholar
  73. Wilson SD, Tilman D (1991) Component of plant competition along an experimental gradient of nitrogen availability. Ecology 72:1050–1065CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Daniel J. Ballhorn
    • 1
  • Adrienne L. Godschalx
    • 1
  • Savannah M. Smart
    • 1
  • Stefanie Kautz
    • 2
  • Martin Schädler
    • 3
  1. 1.Department of BiologyPortland State UniversityPortlandUSA
  2. 2.Department of ZoologyField Museum of Natural HistoryChicagoUSA
  3. 3.Department Community EcologyHelmholtz-Centre for Environmental Research-UFZHalleGermany

Personalised recommendations