, Volume 175, Issue 1, pp 63–72 | Cite as

Experience teaches plants to learn faster and forget slower in environments where it matters

  • Monica GaglianoEmail author
  • Michael Renton
  • Martial Depczynski
  • Stefano Mancuso
Behavioral ecology - Original research


The nervous system of animals serves the acquisition, memorization and recollection of information. Like animals, plants also acquire a huge amount of information from their environment, yet their capacity to memorize and organize learned behavioral responses has not been demonstrated. In Mimosa pudica—the sensitive plant—the defensive leaf-folding behaviour in response to repeated physical disturbance exhibits clear habituation, suggesting some elementary form of learning. Applying the theory and the analytical methods usually employed in animal learning research, we show that leaf-folding habituation is more pronounced and persistent for plants growing in energetically costly environments. Astonishingly, Mimosa can display the learned response even when left undisturbed in a more favourable environment for a month. This relatively long-lasting learned behavioural change as a result of previous experience matches the persistence of habituation effects observed in many animals.


Behaviour Ecological trade-offs Information Anti-predator responses Learning Memory 



We thank Elisa Azzarello and Elisa Masi for assistance with setting up the light environments, and Leigh Simmons, Joseph Tomkins, Anthony Trewavas, Daniel Robert for valuable comments on the manuscript. This study was supported by Research Fellowships from the University of Western Australia and the Australian Research Council to M. G. and research funding from European Commission to S. M.

Supplementary material

442_2013_2873_MOESM1_ESM.pdf (61 kb)
Supplementary material 1 (PDF 66 kb)


  1. Allis CD, Jenuwein T, Reinberg D, Caparros ML (2007) Epigenetics. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  2. Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant Pathol 11:563–576PubMedCrossRefGoogle Scholar
  3. Applewhite PB (1972) Behavioral plasticity in the sensitive plant, Mimosa. Behav Biol 7:47–53PubMedCrossRefGoogle Scholar
  4. Baldwin IT, Schmelz EA (1996) Immunological “memory” in the induced accumulation of nicotine in wild tobacco. Ecology 77:236–246CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42.
  6. Bauer EP, Schafe GE, LeDoux JE (2002) NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22:5239–5249PubMedGoogle Scholar
  7. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Bio 1:11–21CrossRefGoogle Scholar
  8. Bose I, Karmakar R (2008) Simple models of plant learning and memory. Phys Script T106:9–12CrossRefGoogle Scholar
  9. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72PubMedCrossRefGoogle Scholar
  10. Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389PubMedCrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  12. Cahill JF Jr, Bao T, Maloney M, Kolenosky C (2013) Mechanical leaf damage causes localized, but not systematic, changes in leaf movement behaviour of the sensitive plant, Mimosa pudica. Botany 91:43–47CrossRefGoogle Scholar
  13. Chakravarthy SV, Ghosh J (1997) On Hebbian-like adaptation in heart muscle: a proposal for ‘cardiac memory’. Biol Cybern 76:207–215PubMedCrossRefGoogle Scholar
  14. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139PubMedCentralPubMedCrossRefGoogle Scholar
  15. Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395CrossRefGoogle Scholar
  16. Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119CrossRefGoogle Scholar
  17. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  18. Cvrčková F, Lipavská H, Žárský V (2009) Plant intelligence: why, why not or where? Plant Signal Behav 4:394–399PubMedCentralPubMedCrossRefGoogle Scholar
  19. Demongeot J, Thomas R, Thellier M (2000) A mathematical model for storage and recall functions in plants. C R Acad Sci III 323:93–97PubMedCrossRefGoogle Scholar
  20. Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3:740PubMedCrossRefGoogle Scholar
  21. Dostál R (1967) On integration in plants. Harvard University Press, CambridgeGoogle Scholar
  22. Dukas R (2004) Evolutionary biology of animal cognition. Annu Rev Ecol Evol Syst 35:347–374CrossRefGoogle Scholar
  23. Eisenstein EM, Eisenstein D, Smith JC (2001) The evolutionary significance of habituation and sensitization across phylogeny: a behavioural homeostasis model. Integr Phys Behav Sci 36:251–265CrossRefGoogle Scholar
  24. Eisner T (1981) Leaf folding in a sensitive plant: a defensive thorn-exposure mechanism. Proc Natl Acad Sci USA 78:402–404PubMedCentralPubMedCrossRefGoogle Scholar
  25. Esdin J, Pearce K, Glanzman DL (2010) Long-term habituation of the gill-withdrawal reflex in Aplysia requires gene transcription, calcineurin and L-type voltage-gated calcium channels. Front Behav Neurosci 4:181PubMedCentralPubMedCrossRefGoogle Scholar
  26. Fleurat-Lessard P, Bouche-Pillion S, Leloup C, Bonnemain J (1997) Distribution and activity of the plasma membrane H+-ATPase related to motor cell function in Mimosa pudica L. Plant Physiol 114:827–834PubMedCentralPubMedGoogle Scholar
  27. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedCrossRefGoogle Scholar
  28. Gális I, Gaquerel E, Pandey SP, Baldwin IT (2009) Molecular mechanisms underlying plant memory in JA-mediated defence responses. Plant Cell Environ 32:617–627PubMedCrossRefGoogle Scholar
  29. Giles AC, Rankin CH (2009) Behavioral and genetic characterization of habituation using Caenorhabditis elegans. Neurobiol Learn Mem 92:139–146PubMedCrossRefGoogle Scholar
  30. Ginsburg S, Jablonka E (2009) Epigenetic learning in non-neural organisms. J Biosci 33:633–646CrossRefGoogle Scholar
  31. Glanzman DL (2009) Habituation in Aplysia: the Cheshire cat of neuro-biology. Neurobiol Learn Mem 92:147–154PubMedCrossRefGoogle Scholar
  32. Goodrich J, Tweedie S (2002) Remembrance of things past: chromatin remodeling in plant development. Annu Rev Cell Dev Biol 18:707–746PubMedCrossRefGoogle Scholar
  33. Grissom N, Bhatnagar S (2009) Habituation to repeated stress: get used to it. Neurobiol Learn Mem 92:215–224PubMedCentralPubMedCrossRefGoogle Scholar
  34. Halling BD, Aracena-Parks P, Hamilton SL (2005) Regulation of voltage-gated Ca2+ channels by calmodulin. Sci STKE 315:15. doi: 10.1126/stke.3152005re15 Google Scholar
  35. Han S-K, Wagner D (2013) Role of chromatin in water stress responses in plants. J Exp Bot. doi: 10.1093/jxb/ert403 Google Scholar
  36. Hemmi JM, Merkle T (2009) High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc R Soc B 276:4381–4388PubMedCentralPubMedCrossRefGoogle Scholar
  37. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stat Circ 347:1–32Google Scholar
  38. Hoddinott J (1997) Rates of translocation and photosynthesis in Mimosa pudica L. New Phytol 79:269–272CrossRefGoogle Scholar
  39. Inoue J (2008) A simple Hopfield-like cellular network model of plant intelligence. Prog Brain Res 168:169–174PubMedCrossRefGoogle Scholar
  40. Jensen EL, Dill LM, Cahill JF Jr (2011) Applying behavioral-ecological theory to plant defense: light-dependent movement in Mimosa pudica suggests a trade-off between predation risk and energetic reward. Am Nat 177:377–381PubMedCrossRefGoogle Scholar
  41. Karban R (2008) Plant behaviour and communication. Ecol Lett 11:727–739PubMedCrossRefGoogle Scholar
  42. Karban R, Niiho C (1995) Induced resistance and susceptibility to herbivory: plant memory and altered plant development. Ecology 76:1220–1225CrossRefGoogle Scholar
  43. Kawecki TJ (2010) Evolutionary ecology of learning: insights from fruit flies. Popul Ecol 52:15–25CrossRefGoogle Scholar
  44. Kenzer AL, Ghezzi PM, Fuller T (2013) Stimulus specificity and dishabituation of operant responding in humans. J Exp Anal Behav 100:61–78PubMedCrossRefGoogle Scholar
  45. Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21PubMedCentralPubMedCrossRefGoogle Scholar
  46. Kinoshita T, Jacobsen SE (2012) Opening the door to epigenetics in PCP. Plant Cell Physiol 53:763–765PubMedCentralPubMedCrossRefGoogle Scholar
  47. Krasne FB, Teshiba TM (1995) Habituation of an invertebrate escape reflex due to modulation by higher centers rather than local events. Proc Natl Acad Sci USA 92:3362–3366PubMedCentralPubMedCrossRefGoogle Scholar
  48. Ledón-Rettig CC, Richards CL, Martin LB (2013) Epigenetics for behavioral ecologists. Behav Ecol 24:311–324CrossRefGoogle Scholar
  49. Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 227:215–290CrossRefGoogle Scholar
  50. Limback-Stokin K, Korzus E, Nagaoka-Yasuda R, Mayford M (2004) Nuclear calcium/calmodulin regulates memory consolidation. J Neurosci 24:10858–10867PubMedCrossRefGoogle Scholar
  51. Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 422:1046–1049CrossRefGoogle Scholar
  52. Moran N (2007) Osmoregulation of leaf motor cells. FEBS Lett 581:2337–2347PubMedCrossRefGoogle Scholar
  53. Okano H, Hirano T, Balaban E (2000) Learning and memory. Proc Natl Acad Sci USA 97:12403–12404PubMedCentralPubMedCrossRefGoogle Scholar
  54. Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808PubMedCentralPubMedCrossRefGoogle Scholar
  55. Perisse E, Raymond-Delpech V, Neant I, Matsumoto Y, Leclerc C, Moreau M, Sandoz JC (2009) Early calcium increase triggers the formation of olfactory long-term memory in honeybees. BMC Biol 7:30. doi: 10.1186/1741-7007-7-30 PubMedCentralPubMedCrossRefGoogle Scholar
  56. Petrinovich L, Widaman KF (1984) An evaluation of statistical strategies to analyse repeated-measures data. In: Peeke HVS, Petrinovich L (eds) Habituation, sensitization, and behaviour. Academic Press, New York, pp 155–201Google Scholar
  57. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, et al. (2009) Habituation revisited: an updated and revised description of the behavioural characteristics of habituation. Neurobiol Learn Mem 92:135–138PubMedCentralPubMedCrossRefGoogle Scholar
  58. Reyes JC, Hennig L, Gruissem W (2002) Chromatin-remodeling and memory factors. New regulators of plant development. Plant Physiol 130:1090–1101PubMedCentralPubMedCrossRefGoogle Scholar
  59. Roshchina VV (2001) Neurotransmitters in plant life. Science Publishers, EnfieldGoogle Scholar
  60. Ruuhola T, Salminen JP, Haviola S, Yang S, Rantala MJ (2007) Immunological memory of mountain birches: effects of phenolics on performance of the autumnal moth depend on herbivory history of trees. J Chem Ecol 33:1160–1176PubMedCrossRefGoogle Scholar
  61. Shepherd VA (2012) At the root of plant neurobiology. In: Volkov AG (ed) Plant electrophysiology. Springer, Berlin, pp 3–43CrossRefGoogle Scholar
  62. Sung S, Amasino MR (2004) Vernalisation and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10PubMedCrossRefGoogle Scholar
  63. Sztarker J, Tomsic D (2011) Brain modularity in arthropods: individual neurons that support “what” but not “where” memories. J Neurosci 31:8175–8180PubMedCrossRefGoogle Scholar
  64. Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biol 15:1–12PubMedCrossRefGoogle Scholar
  65. Thellier M, Desbiez MO, Champagnat P, Kergosien Y (1982) Do memory processes occur also in plants? Physiol Plant 56:281–284CrossRefGoogle Scholar
  66. Thellier M, Le Sceller L, Norris V, Verdus MC, Ripoll C (2000) Long-distance transport, storage and recall of morphogenetic information in plants: the existence of a primitive plant “memory”. C R Acad Sci III 323:81–91PubMedCrossRefGoogle Scholar
  67. Thompson RF (2009) Habituation: a history. Neurobiol Learn Mem 92:127–134PubMedCentralPubMedCrossRefGoogle Scholar
  68. Thorpe WH (1963) Learning and instinct in animals. Methuen, LondonGoogle Scholar
  69. Tomsic D, de Astrada MB, Sztarker J, Maldonado H (2009) Behavioral and neuronal attributes of short- and long-term habituation in the crab Chasmagnathus. Neurobiol Learn Mem 92:176–182PubMedCrossRefGoogle Scholar
  70. Trewavas T (2003) Aspects of plant intelligence. Ann Bot 92:1–20PubMedCrossRefGoogle Scholar
  71. Tseng AS, Levin M (2013) Cracking the bioelectric code: probing endogenous ionic controls of pattern formation. Commun Integr Biol 6:e22595PubMedCentralPubMedCrossRefGoogle Scholar
  72. Turner CH, Robling AG, Duncan RL, Burr DB (2002) Do bone cells behave like a neuronal network? Calcif Tissue Int 70:435–442PubMedCrossRefGoogle Scholar
  73. Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4PubMedCentralPubMedCrossRefGoogle Scholar
  74. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118PubMedCrossRefGoogle Scholar
  75. Volkov AG, Carrell H, Adesina T, Markin VS, Jovanov E (2008) Plant electrical memory. Plant Signal Behav 3:490–492PubMedCentralPubMedCrossRefGoogle Scholar
  76. Wiel DE, Weeks JC (1996) Habituation and dishabituation of the proleg withdrawal reflex in larvae of the sphinx hawk, Manduca sexta. Behav Neurosci 110:1133–1147PubMedCrossRefGoogle Scholar
  77. Yaish MW, Colasanti J, Rothstein SJ (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62:3727–3735PubMedCrossRefGoogle Scholar
  78. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512PubMedCrossRefGoogle Scholar
  79. Yellen G (1998) The moving parts of voltage-gated ion channels. Q Rev Biophys 31:239–295PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Monica Gagliano
    • 1
    Email author
  • Michael Renton
    • 2
  • Martial Depczynski
    • 3
  • Stefano Mancuso
    • 4
  1. 1.Centre for Evolutionary Biology, School of Animal BiologyUniversity of Western AustraliaCrawleyAustralia
  2. 2.School of Plant BiologyUniversity of Western AustraliaCrawleyAustralia
  3. 3.AIMS, The Oceans InstituteUniversity of Western AustraliaCrawleyAustralia
  4. 4.LINV, Department of Plant, Soil and Environmental ScienceUniversity of FirenzeFirenzeItaly

Personalised recommendations