Evolutionary Ecology

, Volume 31, Issue 6, pp 913–923 | Cite as

Fruit defence syndromes: the independent evolution of mechanical and chemical defences

  • Omer NevoEmail author
  • Kim Valenta
  • Alex G. Tevlin
  • Patrick Omeja
  • Sarah A. Styler
  • Derek J. Jackson
  • Colin A. Chapman
  • Manfred Ayasse
Original Paper


Plants are prone to attack by a great diversity of antagonists against which they deploy various defence mechanisms, of which the two principle ones are mechanical and chemical defences. These defences are hypothesized to be negatively correlated due to either functional redundancy or a trade-off, i.e., plants which rely on increased mechanical defence should downregulate their degree of chemical defence and vice versa. A competing hypothesis is that different defences perform distinct functions and draw from different pools of resources, which should result in their independent evolution. We examine these competing hypotheses using two independent datasets of fleshy fruits we collected from Madagascar and Uganda. We sampled mechanical defences, indexed by fruit puncture resistance, and defensive defences, indexed by defensive volatile organic compounds, and examined their associations using phylogenetically-controlled models. In both systems, we found no correlation between mechanical and chemical defences, thus supporting the independent evolution hypothesis. This implies that fruit defence mechanisms reflect a more complex array of selection pressures and constraints than previously perceived.


Animal-plant interactions Fleshy fruits Mechanical defence Chemical defence Constraints Trade-off 



We thank Lisa A. D’Agostino for her assistance in conducting the chemical analysis. We thank the Canada Research Chairs Program, Natural Science and Engineering Research Council of Canada, Fonds Québécois de la Recherche sur la Nature et les Technologies, the National Geographic Society for funding. ON was funded by a German Science Foundation grant (NE 2156/1-1) while working on this manuscript. We thank MICET and Madagascar National Parks, for permission to conduct this research in Madagascar. We are grateful to Paul Tsiveraza, Francette, Mamy Razafitsalama and Jean de-la-Dieu for contributions in the field.

Supplementary material

10682_2017_9919_MOESM1_ESM.png (2.6 mb)
Supplementary material 1 (PNG 2699 kb)
10682_2017_9919_MOESM2_ESM.xls (60 kb)
Supplementary material 2 (XLS 60 kb)
10682_2017_9919_MOESM3_ESM.xls (74 kb)
Supplementary material 3 (XLS 74 kb)


  1. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:132–149. doi: 10.1890/0012-9658(2006)87[132:PDS]2.0.CO;2Google Scholar
  2. Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991. doi: 10.1111/ele.12482 CrossRefPubMedGoogle Scholar
  3. Aguirre LF, Herrel A, Van Damme R, Matthysen E (2003) The implications of food hardness for diet in bats. Funct Ecol 17:201–212. doi: 10.1046/j.1365-2435.2003.00721.x CrossRefGoogle Scholar
  4. Ballhorn DJ, Godschalx AL, Kautz S (2013) 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 CrossRefPubMedGoogle Scholar
  5. Ballhorn DJ, Godschalx AL, Smart SM et al (2014) Chemical defense lowers plant competitiveness. Oecologia 176:811–824. doi: 10.1007/s00442-014-3036-1 CrossRefPubMedGoogle Scholar
  6. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745Google Scholar
  7. Chapman CA, Chapman LJ (2002) Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comp Biochem Physiol Part A 133:861–875CrossRefGoogle Scholar
  8. Chen X, Cannon CH, Conklin-Brittan NL (2012) Evidence for a trade-off strategy in stone oak (Lithocarpus) seeds between physical and chemical defense highlights fiber as an important antifeedant. PLoS ONE 7:1–9. doi: 10.1371/journal.pone.0032890 Google Scholar
  9. Cipollini ML (2000) Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev Chil Hist Nat 73:421–440CrossRefGoogle Scholar
  10. Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372CrossRefPubMedGoogle Scholar
  11. Cipollini ML, Paulk E, Mink K et al (2004) Defense tradeoffs in fleshy fruits: effects of resource variation on growth, reproduction, and fruit secondary chemistry in Solanum carolinense. J Chem Ecol 30:1–17. doi: 10.1023/B:JOEC.0000013179.45661.68 CrossRefPubMedGoogle Scholar
  12. Eichenberg D, Purschke O, Ristok C et al (2015) Trade-offs between physical and chemical carbon-based leaf defence: of intraspecific variation and trait evolution. J Ecol 103:1667–1679. doi: 10.1111/1365-2745.12475 CrossRefGoogle Scholar
  13. Ellenbogen JM, Payne JD, Stickgold R (2006) The role of sleep in declarative memory consolidation: passive, permissive, active or none? Curr Opin Neurobiol 16:716–722. doi: 10.1016/j.conb.2006.10.006 CrossRefPubMedGoogle Scholar
  14. Eriksson O, Ehrlén J (1998) Secondary metabolites in fleshy fruits: are adaptive explanations needed? Am Nat 152:905–907CrossRefPubMedGoogle Scholar
  15. Farmer EE (2014) Leaf defence. Oxford University Press, OxfordCrossRefGoogle Scholar
  16. Fischbach MA, Clardy J (2007) One pathway, many products. Nat Chem Biol 3:353–355CrossRefPubMedGoogle Scholar
  17. Follett PA (2017) Insect-plant interactions: host selection, herbivory, and plant resistance - an introduction. Entomol Exp Appl 162:1–3. doi: 10.1111/eea.12524 CrossRefGoogle Scholar
  18. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414. doi: 10.1038/nchembio.2007.5 CrossRefPubMedGoogle Scholar
  19. Gipenberg S, Rota J, Kim J et al (2017) Seed polyphenols in a diverse tropical plant community. J Ecol. doi: 10.1111/1365-2745.12814 Google Scholar
  20. Gonçalves MF, Malheiro R, Casal S et al (2012) Influence of fruit traits on oviposition preference of the olive fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), on three Portuguese olive varieties (Cobrancosa, Madural and Verdeal Transmontana). Sci Hortic (Amsterdam) 145:127–135. doi: 10.1016/j.scienta.2012.08.002 CrossRefGoogle Scholar
  21. Hamilton AC (1981) A field guide to Uganda forest trees. Makerere University Printery, KampalaGoogle Scholar
  22. Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133. doi: 10.1016/S1360-1385(00)01556-9 CrossRefPubMedGoogle Scholar
  23. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. doi: 10.1086/417659 CrossRefGoogle Scholar
  24. Herrera CM (1982) Defense of ripe fruit from pests: its significance in relation to plant-disperser interactions. Am Nat 120:218–241CrossRefGoogle Scholar
  25. Hodgkison R, Ayasse M, Häberlein C et al (2013) Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the New and Old World tropics. Funct Ecol 27:1075–1084. doi: 10.1111/1365-2435.12101 CrossRefGoogle Scholar
  26. Jacobs GH (2009) Evolution of colour vision in mammals. Philos Trans R Soc Lond B Biol Sci 364:2957–2967. doi: 10.1098/rstb.2009.0039 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kariñho-Betancourt E, Agrawal AA, Halitschke R, Núñez-Farfán J (2015) Phylogenetic correlations among chemical and physical plant defenses change with ontogeny. New Phytol 206:796–806. doi: 10.1111/nph.13300 CrossRefPubMedGoogle Scholar
  28. Kessler A, Baldwin IT (2000) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. doi: 10.1126/science.291.5511.2141 Google Scholar
  29. Koricheva J, Nykänen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75. doi: 10.1086/382601 CrossRefPubMedGoogle Scholar
  30. Lambert JE, Chapman CA, Wrangham RW, Lou Conklin-Brittain N (2004) Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125:363–368. doi: 10.1002/ajpa.10403 CrossRefPubMedGoogle Scholar
  31. Lasa R, Tadeo E, Dinorín LA et al (2017) Fruit firmness, superficial damage, and location modulate infestation by Drosophila suzukii and Zaprionus indianus: the case of guava in Veracruz, Mexico. Entomol Exp Appl 162:4–12. doi: 10.1111/eea.12519 CrossRefGoogle Scholar
  32. Lomáscolo SB, Levey DJ, Kimball RT et al (2010) Dispersers shape fruit diversity in Ficus (Moraceae). PNAS 107:14668–14672. doi: 10.1073/pnas.1008773107 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. Nevo O, Heymann EW, Schulz S, Ayasse M (2016) Fruit odor as a ripeness signal for seed-dispersing primates? a case study on four Neotropical plant species. J Chem Ecol 42:323–328. doi: 10.1007/s10886-016-0687-x CrossRefPubMedPubMedCentralGoogle Scholar
  35. Orme D, Freckleton RP, Thomas G, et al. (2012) Caper: comparative analyses of phylogenetics and evolution in R. R package version 0.5Google Scholar
  36. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  37. Pellmyr O, Thien LB (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35:76–85CrossRefGoogle Scholar
  38. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  39. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223CrossRefGoogle Scholar
  40. Rodríguez A, Alquézar B, Peña L (2013) Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol 197:36–48. doi: 10.1111/j.1469-8137.2012.04382.x CrossRefPubMedGoogle Scholar
  41. Schaefer HM, Ruxton GD (2011) Animal-plant communication. Oxford University Press, OxfordCrossRefGoogle Scholar
  42. Schaefer HM, Schmidt V, Winkler H (2003) Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos 102:318–328. doi: 10.1034/j.1600-0706.2003.11796.x CrossRefGoogle Scholar
  43. Schatz GE (2001) Generic tree flora of Madagascar. Royal Botanic Gardens, KewGoogle Scholar
  44. Stamopoulos DC, Damos P, Karagianidou G (2007) Bioactivity of five monoterpenoid vapours to Tribolium confusum (du Val) (Coleoptera: Tenebrionidae). J Stored Prod Res 43:571–577. doi: 10.1016/j.jspr.2007.03.007 CrossRefGoogle Scholar
  45. Takahara B, Takahashi KH (2017) Associative learning of color and firmness of oviposition substrates in Drosophila suzukii. Entomol Exp Appl 162:13–18. doi: 10.1111/eea.12521 CrossRefGoogle Scholar
  46. Tiansawat P, Davis AS, Berhow MA et al (2014) Investment in seed physical defence is associated with species’ light requirement for regeneration and seed persistence: evidence from Macaranga species in Borneo. PLoS ONE. doi: 10.1371/journal.pone.0099691 PubMedPubMedCentralGoogle Scholar
  47. Twigg LE, Socha LV (1996) Physical versus chemical defence mechanisms in toxic Gastrolobium. Oecologia 108:21–28. doi: 10.1007/BF00333210 CrossRefPubMedGoogle Scholar
  48. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485. doi: 10.1016/j.pbi.2009.04.001 CrossRefPubMedGoogle Scholar
  49. Valenta K, Brown KA, Rafaliarison RR et al (2015) Sensory integration during foraging: the importance of fruit hardness, colour, and odour to brown lemurs. Behav Ecol Sociobiol. doi: 10.1007/s00265-015-1998-6 Google Scholar
  50. Valenta K, Nevo O, Martel C, Chapman CA (2017) Plant attractants: integrating insights from seed dispersal and pollination ecology. Evol Ecol 31:249. doi: 10.1007/s10682-016-9870-3 CrossRefGoogle Scholar
  51. Vorobyev M, Osorio D, Bennett ATD et al (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol 183:621–633CrossRefGoogle Scholar
  52. Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183. doi: 10.1111/j.1471-8286.2004.00829.x CrossRefGoogle Scholar
  53. Westbrook JW, Kitajima K, Burleigh JG et al (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a Neotropical forest. Am Nat 177:800–811. doi: 10.1086/659963 CrossRefPubMedGoogle Scholar
  54. Whitehead SR, Obando Quesada MF, Bowers MD (2015) Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats. Oikos 125:927–937. doi: 10.1111/oik.02210 CrossRefGoogle Scholar
  55. Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am Nat 147:599–608CrossRefGoogle Scholar
  56. Zanne AE, Tank DC, Cornwell WK et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92. doi: 10.1038/nature12872 CrossRefPubMedGoogle Scholar
  57. Zhang Z, Wang Z, Chang G et al (2016) Trade-off between seed defensive traits and impacts on interaction patterns between seeds and rodents in forest ecosystems. Plant Ecol 217:253–265. doi: 10.1007/s11258-016-0566-0 CrossRefGoogle Scholar
  58. Zhao D, Reddy KR, Kakani VG, Reddy VR (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. Eur J Agron 22:391–403. doi: 10.1016/j.eja.2004.06.005 CrossRefGoogle Scholar
  59. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:10–11. doi: 10.1146/annurev-arplant-042916-040856 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  2. 2.McGill School of the Environment, Department of AnthropologyMcGill UniversityMontrealCanada
  3. 3.Department of ChemistryUniversity of TorontoTorontoCanada
  4. 4.Makerere University Biological Field StationKampalaUganda
  5. 5.Department of ChemistryUniversity of AlbertaEdmontonCanada
  6. 6.Department of ChemistryYork UniversityTorontoCanada

Personalised recommendations