, Volume 172, Issue 4, pp 1051–1060 | Cite as

Glandular trichomes as an inflorescence defence mechanism against insect herbivores in Iberian columbines

  • Rafael Jaime
  • Pedro J. ReyEmail author
  • Julio M. Alcántara
  • Jesús M. Bastida
Plant-animal interactions - Original research


Glandular trichomes play a defensive role against herbivores in the leaves of many plant species. However, their functional role in inflorescences has not been studied, even though theory suggests that tissues with a higher fitness value, such as inflorescences, should be better defended. Using manipulative experiments, we analysed the defensive role of glandular trichomes against herbivorous insects in the inflorescence of Iberian columbines (genus Aquilegia), and its inter-population and inter-taxa variation in relation to herbivore abundance and potential selective pressure. The experiments were conducted in eight populations belonging to four subspecies of two columbines (Aquilegia vulgaris and Aquilegia pyrenaica). For each population, we estimated the density of glandular trichomes in the inflorescences, the abundance of insects stuck in the inflorescences, the abundance of small herbivorous insects, the incidence of damage on flowers and fruits, and the fruit set. The density of glandular trichomes on the inflorescence of A. vulgaris and A. pyrenaica was higher in regions of higher herbivore abundance. We also found that when the plants lose the protection of glandular trichomes, small insects have better access to flowers and fruits, causing more damage and reducing plant fitness. This study concludes that glandular trichomes are part of an adaptive response against phytophagous insect herbivory. The observed variation in herbivore pressure between taxa, likely caused by habitat differentiation, might have played a role in trait differentiation through divergent selection. This result adds evidence to the differentiation of the Iberian columbines through habitat specialization.


Adaptation Phytophagous insects Herbivory Natural selection Trichomes 



We are grateful to Gloria M. Galiano Gonzalez and Ana Marchal Bermudez for their assistance in fieldwork. During the development of this study, the authors were supported by the Spanish Ministerio de Ciencia e Innovación (MICINN) projects CGL2006-02848 and CGL2009-08130, including Fonds européen de développement régional of the European Commission. During this study, RJ was supported by grant BES-2007-16060 of the MICINN.

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  1. Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279:1201–1202PubMedCrossRefGoogle Scholar
  2. Alcántara JM, Bastida JM, Rey PJ (2010) Linking divergent selection on vegetative traits to environmental variation and phenotypic diversification in the Iberian columbines (Aquilegia). J Evol Biol 2:1218–1233CrossRefGoogle Scholar
  3. Bastida JM, Alcántara JM, Rey PJ, Vargas P, Herrera CM (2010) Extended phylogeny of Aquilegia: the biogeographical and ecological patterns of two simultaneous but contrasting radiations. Plant Syst Evol 284:171–185CrossRefGoogle Scholar
  4. Belcher DW, Thurston R (1982) Inhibition of movement of larvae of the convergent lady beetle by leaf trichomes of tobacco. Environ Entomol 11:91–94Google Scholar
  5. Berenbaum MR, Zangerl AR (1998) Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci USA 95:13743–13748PubMedCrossRefGoogle Scholar
  6. Blanché C, Molero J (1986) Delphinium L. In: Castroviejo S, Laínz M, López G, Monserrat P, Muñoz F, Paiva J, Villar L (eds) Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, vol I. Real Jardín Botánico, Servicio de Publicaciones del CSIC, Madrid, pp 242–251Google Scholar
  7. Brenes-Arguedas T, Coley PD, Kursar TA (2008) Divergence and diversity in the defensive ecology of Inga at two Neotropical sites. J Ecol 96:127–135Google Scholar
  8. Buta JG, Lusby WR, Neal JW (1993) Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporariorum. Phytochemistry 32:859–864CrossRefGoogle Scholar
  9. Castellanos MC, Alcántara JM, Rey PJ, Bastida JM (2011) Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations. Mol Ecol 20:3513–3524PubMedGoogle Scholar
  10. Cipollini DF, Bergelson J (2002) Plant density and nutrient availability constrain constitutive and wound-induced expression of trypsin inhibitors in Brassica napus. J Chem Ecol 27:593–610CrossRefGoogle Scholar
  11. Devesa JA (2000) Ononis L. In: Talavera S, Aedo C, Castroviejo S, Herrero A, Romero Zarco C, Salgueiro FJ, Velayos M (eds) Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, vol VII (II). Real Jardín Botánico, Servicio de Publicaciones del CSIC, Madrid, pp 590–646Google Scholar
  12. Díaz González TE (1986) Aquilegia L. In: Castroviejo S, Laínz M, López G, Monserrat P, Muñoz F, Paiva J, Villar L (eds) Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, vol I. Real Jardín Botánico, Servicio de Publicaciones del CSIC, Madrid, pp 376–387Google Scholar
  13. Ehleringer JR, Bjorkman O, Mooney HA (1976) Leaf pubescence: effects on absorbance and photosynthesis in a desert shrub. Science 192:376–377PubMedCrossRefGoogle Scholar
  14. Elle E, Hare JD (2000) No benefit of glandular trichome production in natural populations of Datura wrightii. Oecologia 123:57–65CrossRefGoogle Scholar
  15. Hare JD, Smith JL (2005) Competition, herbivory, and reproduction of trichome phenotypes of Datura wrightii. Ecology 86:334–339CrossRefGoogle Scholar
  16. Hartvigsen G, McNaughton SJ (1995) Trade off between height and relative growth rate in a dominant grass from the Serengeti ecosystem. Oecologia 102:273–276CrossRefGoogle Scholar
  17. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Syst 34:425–453CrossRefGoogle Scholar
  18. Hodges SA, Fulton M, Yang JY, Whittall JB (2004) Research review. Verne Grant and evolutionary studies of Aquilegia. New Phytol 161:113–120CrossRefGoogle Scholar
  19. Holeski LM (2007) PhD dissertation. Quantitative trait evolution in Mimulus guttatus (yellow monkeyflower). Department of Ecology and Evolutionary Biology, University of Kansas, LawrenceGoogle Scholar
  20. Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503CrossRefGoogle Scholar
  21. Janzen DH (1973) Dissolution of mutualism between Cecropia and its Azteca ants. Biotropica 5:15–28CrossRefGoogle Scholar
  22. Karabourniotis G, Papadopoulos K, Papamarkou M, Manetas Y (1992) Ultraviolet-B radiation absorbing capacity of leaf hairs. Physiol Plant 86:414–418CrossRefGoogle Scholar
  23. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  24. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in while tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  25. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatiles emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  26. Koptur S (1984) Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65:1787–1793CrossRefGoogle Scholar
  27. Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE, Weber MG, Murakami ET, Drake C, McGregor R, Coley PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci 106:18073–18078PubMedCrossRefGoogle Scholar
  28. Lambert AM (2007) Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator. Arthropod-Plant Interact 1:167–173CrossRefGoogle Scholar
  29. Lavergne S, Debussche M, Thompson JD (2005) Limitations on reproductive success in endemic Aquilegia viscosa (Ranunculaceae) relative to its widespread congener Aquilegia vulgaris: the interplay of herbivory and pollination. Oecologia 142:212–220PubMedCrossRefGoogle Scholar
  30. Lemke CA, Mutschler MA (1984) Inheritance of glandular trichomes in crosses between Lycopersicon esculentum and Lycopersicon pennellii. J Am Soc Hortic Sci 109:592–596Google Scholar
  31. Levin DA (1973) The role of trichomes in plant defense. Q R Biol 48:3–15CrossRefGoogle Scholar
  32. Lovinger A, Liewehr D, Lamp O (2000) Glandular trichomes on alfalfa impede searching behavior of the potato leafhopper parasitoid. Biol Control 18:187–192CrossRefGoogle Scholar
  33. Marquis RJ (1992) Selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, Chicago, pp 301–325Google Scholar
  34. Martin C, Glover BJ (2007) Functional aspects of cell patterning in aerial epidermis. Curr Opin Plant Biol 10:70–82PubMedCrossRefGoogle Scholar
  35. Mauricio R (1998) Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Nat 151:20–28PubMedCrossRefGoogle Scholar
  36. McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320CrossRefGoogle Scholar
  37. McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 55–133Google Scholar
  38. Medrano M, Castellanos MC, Herrera CM (2006) Comparative floral and vegetative differentiation between two European Aquilegia taxa along a narrow contact zone. Plant Syst Evol 262:209–224CrossRefGoogle Scholar
  39. Nogueira A, Rey PJ, Lohmann LG (2012) Evolution of extrafloral nectaries: adaptive process and selective regime changes from forest to savanna. J Evol Biol 25(11):2325–2340PubMedCrossRefGoogle Scholar
  40. Nold R (2003) Columbines. Aquilegia, Paraquilegia and Semiaquilegia. Timber Press, CambridgeGoogle Scholar
  41. 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 3–54Google Scholar
  42. Romero GQ, Souza JS, Vasconcellos-Neto J (2008) Anti-herbivore protection by mutualistic spiders and the role of plant glandular trichomes. Ecology 89:3105–3115CrossRefGoogle Scholar
  43. Schluter D (2000) The ecology of adaptive radiation. Oxford Series in Ecology and Evolution. Oxford University Press, New YorkGoogle Scholar
  44. StatSoft, Inc. 2004. STATISTICA (data analysis software system), version 7.
  45. Strauss S, Zangerl AR (2002) Plant–insect interactions in terrestrial ecosystems. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions. An evolutionary approach. Blackwell Science, Oxford, UK, pp 77–106Google Scholar
  46. Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532CrossRefGoogle Scholar
  47. Treacy MF, Benedict JH, Segers JC, Morrison RK, Lopez JD (1986) Role of cotton trichome density in bollworm (Lepidoptera: Noctuidae) egg parasitism. Environ Entomol 15:365–368Google Scholar
  48. Treacy MF, Benedict JH, Lopez JD, Morrison RK (1987) Functional response of a predator (Neuroptera: Chrysopidae) to bollworm (Lepidoptera: Noctuidae) eggs on smoothleaf, hirsute, and pilose cottons. J Econ Entomol 80:376–379Google Scholar
  49. Valverde PL, Fornoni J, Nuñez-Farfán J (2001) Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J Evol Biol 14:424–432CrossRefGoogle Scholar
  50. Van Dam NM, Hare JD, Elle E (1999) Inheritance and distribution of trichome phenotypes in Datura wrightii. J Hered 90:220–227CrossRefGoogle Scholar
  51. Vogelmann TC (1993) Plant-tissue optics. Annu Rev Plant Physiol Plant Mol Biol 44:231–251CrossRefGoogle Scholar
  52. Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96:675–679PubMedCrossRefGoogle Scholar
  53. Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93:3–11PubMedCrossRefGoogle Scholar
  54. Wang E, Wang R, De Parasis J, Loughrin JH, Gan S, Wagner GJ (2001) Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat Biotechnol 19:371–374PubMedCrossRefGoogle Scholar
  55. War AR, Sharma HC, Paulraj MG, War MY, Ignacimuthu S (2011) Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav 6:1973–1978PubMedCrossRefGoogle Scholar
  56. Yan A, Pan J, An L, Gan Y, Feng H (2012) The response of trichomes mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. J Phtochem Photobiol B Biol 113:29–35CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Rafael Jaime
    • 1
  • Pedro J. Rey
    • 1
    Email author
  • Julio M. Alcántara
    • 1
  • Jesús M. Bastida
    • 2
  1. 1.Departamento de Biología Animal, Biología Vegetal y EcologíaUniversidad de JaénJaénSpain
  2. 2.Laboratorio Ecología y Evolución de Polinización y Sistemas Reproductivos en Plantas, Centro de Investigaciones en EcosistemasUniversidad Nacional Autónoma de MéxicoMoreliaMexico

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