Skip to main content

Plant intelligence

Naturwissenschaften volume 92, pages 401–413 (2005)Cite this article

Abstract

Intelligent behavior is a complex adaptive phenomenon that has evolved to enable organisms to deal with variable environmental circumstances. Maximizing fitness requires skill in foraging for necessary resources (food) in competitive circumstances and is probably the activity in which intelligent behavior is most easily seen. Biologists suggest that intelligence encompasses the characteristics of detailed sensory perception, information processing, learning, memory, choice, optimisation of resource sequestration with minimal outlay, self-recognition, and foresight by predictive modeling. All these properties are concerned with a capacity for problem solving in recurrent and novel situations. Here I review the evidence that individual plant species exhibit all of these intelligent behavioral capabilities but do so through phenotypic plasticity, not movement. Furthermore it is in the competitive foraging for resources that most of these intelligent attributes have been detected. Plants should therefore be regarded as prototypical intelligent organisms, a concept that has considerable consequences for investigations of whole plant communication, computation and signal transduction.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Aarsen LW (1995) Hypotheses for the evolution of apical dominance in plants: implications for the interpretation of overcompensation. Oikos 74:149–156

    Google Scholar 

  • Ackerley DD, Bazzaz FA (1995) Seedling crown orientation and interception of diffuse radiation in tropical forest gaps. Ecology 76:1134–1146

    Google Scholar 

  • Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401:60–63

    Article  CAS  Google Scholar 

  • Allmann JM (1999) Evolving Brains. Scientific American Library, New York

    Google Scholar 

  • Amzallag GN, Lerner HR, Poljakoff-Mayber A (1990) Induction of increased salt tolerance in Sorghum bicolor by sodium chloride treatment. J Exp Bot 41:29–34

    CAS  Google Scholar 

  • Aphalo PJ, Ballare CL (1995) On the importance of information-acquiring systems in plant–plant interactions. Funct Ecol 9:5–14

    Google Scholar 

  • Appleby AP (1998) The practical implications of hormetic effects of herbicides on plants. Human Exp Toxicol 17:270–271

    Article  CAS  Google Scholar 

  • Appleby AP, Olsen PD, Colbert DR (1976) Winter wheat yield reductions from interference by Italian ryegrass. Agron J 68:463–466

    Article  Google Scholar 

  • Arkin A, Ross J (1994) Computational functions in biochemical reaction networks. Biophys J 67:560–578

    PubMed  CAS  Google Scholar 

  • Attenborough D (1995) The Private Life of Plants. BBC Natural History Unit, British Broadcasting Corporation, London. TV production in association with Turner Broadcasting Systems Inc., London

    Google Scholar 

  • Baillaud L (1962) Mouvements autonomes des tiges, vrilles et autre organs. In: Ruhland W (ed) Encyclopedia plant physiol: XVII. Physiology of movements, part 2. Springer-Verlag, Berlin Hedilberg New York, pp 562–635

    Google Scholar 

  • Baker AJM, Grant CJ, Martin MH, Shaw SC, Whitebrook J (1985) Induction and loss of cadmium tolerance in Holcus lanatus and other grasses. New Phytol 102:575–587

    Google Scholar 

  • Ballare CL (1994) Light gaps: sensing the light opportunities in highly dynamic canopy environments. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York, pp 73–111

    Google Scholar 

  • Ballare CL (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci 4:97–102

    Article  PubMed  Google Scholar 

  • Bazzaz FA (1996) Plants in Changing Environments. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Bell G, Lechowicz MJ (1994) Spatial heterogeneity at small scales and how plants respond to it. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York,pp 391–411

    Google Scholar 

  • Bennet-Clark TA, Ball NG (1951) The diageotropic behavior of rhizomes. J Exp Bot 2:169–203

    Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Ann Rev Ecol Syst 16:363–392

    Google Scholar 

  • Bonabeau E, Dorigo M, Theraulax G (2000) Inspiration for optimisation from social insect behavior. Nature 406:39–42

    Article  PubMed  CAS  Google Scholar 

  • Bonabeau E, Meyer C (2001) Swarm intelligence. Harvard Business Review, May 2001, 107–114

  • Bonabeau E, Theraulaz G (2000) Swarm Smarts. Scientific American 282:72

    PubMed  CAS  Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity. Adv Genet 13:115–155

    Google Scholar 

  • Bray D (1995) Protein molecules as computational elements in living cells. Nature 376:307–312

    Article  PubMed  CAS  Google Scholar 

  • Brown H, Martin MH (1981) Pre-treatment effects of cadmium on the root growth of Holcus lanatus. New Phytol 89:621–629

    CAS  Google Scholar 

  • Cairns J, Overbaugh J, Miller S (1988) The origin of mutants. Nature 335:142–145

    Article  PubMed  CAS  Google Scholar 

  • Calabrese EJ, Baldwin LA (2001) Hormesis: U-shaped dose responses and their centrality in toxicology. Trends Pharmacol Sci 22:285–291

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128

    Google Scholar 

  • Cannon WB (1932) The wisdom of the body. Norton, New York

    Google Scholar 

  • Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136

    Article  PubMed  CAS  Google Scholar 

  • Corning P (2003) Nature's Magic-synergy in evolution and the fate of humankind. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. John Murray, London

    Google Scholar 

  • Darwin C (1882) The power of movement in plants. John Murray, London

    Google Scholar 

  • Darwin C (1891) The movements and habits of climbing plants. John Murray, London

    Google Scholar 

  • Darwinkel A (1978) Patterns of tillering and grain production of winter wheat at a wide range of plant densities. Neth J Agric Sci 26:383–398

    Google Scholar 

  • De Castro LN, Timmis JI (2002) Artificial immune systems : a new computational intelligence approach. Springer-Verlag, London

    Google Scholar 

  • De Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143–152

    Google Scholar 

  • Desbiez MO, Kergosein Y, Champagnant P, Thellier M (1984) Memorisation and delayed expression of regulatory message in plants. Planta 160:392–399

    Article  Google Scholar 

  • Desbiez MO, Tort M, Thellier M (1991) Control of a symmetry breaking process in the course of morphogenesis of plantlets of Bidens pilosa. Planta 184:397–402

    Article  Google Scholar 

  • Drew MC, Saker LR (1975) Nutrient supply and the growth of the seminal root system in barley. J Exp Bot 26:79–90

    CAS  Google Scholar 

  • Durrant A (1962) The environmental induction of heritable change in Linum. Heredity 17:27–61

    Google Scholar 

  • Durrant A (1981) Unstable genotypes. Phil Trans R Soc Lond Ser B Biol Sci 292:467–474

    CAS  Google Scholar 

  • Eapen D, Barroso ML, Campos ME, Ponce G, Corkidi G, Dubrovsky JG, Cassab GI (2003) A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis. Plant Physiol 131:536–546

    Article  PubMed  CAS  Google Scholar 

  • Evans JP, Cain ML (1995) A spatially explicit test of foraging behavior in a clonal plant. Ecology 76:1147–1155

    Google Scholar 

  • Falik O, Reides P, Gersani M, Novoplansky A (2003) Self, non-self discrimination in roots. J Ecol 91:525–531

    Article  Google Scholar 

  • Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696

    Article  Google Scholar 

  • Franco M (1986) The influence of neighbours on the growth of modular organisms with an example from trees. Phil Trans R Soc Lond Ser B Biol Sci 313:209–225

    Google Scholar 

  • Franks NR, Dornhaus A, Fitzsimmons JP, Stevens M (2003) Speed versus accuracy in collective decision-making. Proc R Soc Lond Ser B Biol Sci 270:2457–2463

    Article  Google Scholar 

  • Gavin AC, Bosche M, Krause R, et al. (2002) Functional organisation of the yeast proteome by systematic analysis of protein complexes. Nature 415:541–547

    Article  PubMed  Google Scholar 

  • Geber MA, Watson MA, De Kroon H (1997) Organ preformation, development and resource allocation in perennials. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic London,pp 113–143

    Google Scholar 

  • Gersani M, Abramsky Z, Falik O (1998) Density-dependent habitat selection in plants. Evol Ecol 12:223–234

    Article  Google Scholar 

  • Gersani M, Brown JS, O'Brien EE, Maina GM, Abramsky Z (2001) Tragedy of the commons as a result of root competition. Ecol 89:660–669

    Article  Google Scholar 

  • Gersani M, Sachs T (1992) Developmental correlations between roots in heterogenous environments. Plant Cell Environ 15:463–499

    Google Scholar 

  • Gilroy S, Trewavas AJ (2001) Signal processing and transduction in plant cells: the end of the beginning? Nature Mol Cell Biol Rev 2:307–314

    Article  CAS  Google Scholar 

  • Givnish TJ (1982) On the adaptive significance of leaf height in forest herbs. Am Naturalist 120:353–381

    Article  Google Scholar 

  • Gleeson SK, Fry JE (1997) Root proliferation and marginal patch value. Oikos 79:387–393

    Google Scholar 

  • Goldberg DE, Barton AM (1992) Patterns and consequences of interspecific competition within natural communities: a review of field experiments with plants. Am Naturalist 139:771–801

    Article  Google Scholar 

  • Goodwins R (2001) The machine that wanted to be a mind. ZDNet UK, January 23

  • Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Harvard, MA

    Google Scholar 

  • Granato TC, Raper CD (1989) Proliferation of maize roots in response to localised supply of nitrate. J Exp Bot 40:263–275

    PubMed  CAS  Google Scholar 

  • Greengard P (2001) The neurobiology of slow synaptic transmission. Science 294:1024–1030

    Article  PubMed  CAS  Google Scholar 

  • Grime JP (1994) The role of plasticity in exploiting environmental heterogeneity. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York, pp 1–19

    Google Scholar 

  • Grime JP, Crick JC, Rincon JE (1986) The ecological significance of plasticity. In: Jennings DH, Trewavas AJ, (eds) Symp Soc Exptl Biol Med XL. Plasticity in Plants. Cambridge University Press,London,pp 5–29

    Google Scholar 

  • Groseburg RK, Hart MW (2000) Mate selection and the evolution of highly polymorphic self/non self recognition genes. Science 289:2111–2114

    Article  PubMed  Google Scholar 

  • Gruntman M, Novoplansky A (2004) Physiologically mediated self/non self discrimination mechanism. Proc Natl Acad Sci USA 101:3863–3867

    Article  PubMed  CAS  Google Scholar 

  • Harper JL (1977) The population biology of plants. Academic, London

    Google Scholar 

  • Hartnett DC, Bazzaz FA (1983) Physiological integration among intra-clonal ramets in Solidago canadensis. Ecol 64:779–788

    Google Scholar 

  • Hartnett DC, Bazzaz FA (1985) The integration of neighbourhood effects inclonal genets of Solidago candensis. J Ecol 73:415–427

    Google Scholar 

  • Hellmeier H, Erhard M, Schulze ED (1997) Biomass accumulation and water use under arid conditions. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic, London,pp 93–113

    Google Scholar 

  • Henrikkson J (2001) Differential shading of branches or whole trees: survival, growth and reproduction. Oecologia 126:482–486

    Article  Google Scholar 

  • Henslow G (1895) The origin of plant structures by self adaptation to the environment. Kegan, Paul, French, Trubner and Co., London

    Google Scholar 

  • Holzapfel C, Alpert P (2003) Root co-operation in a clonal plant: connected strawberries segregate roots. Oecologia 134:72–77

    Article  PubMed  Google Scholar 

  • Honda H, Fisher JB (1978) Tree branch angle: maximising effective leaf area. Science 199:888–889

    PubMed  CAS  Google Scholar 

  • Honkanen T, Hanioja E (1994) Why does a branch suffer more after branch-wide than after tree-wide defoliation? Oikos 71:441–450

    Google Scholar 

  • Huber-Sannwald E, Pyke DA, Caldwell MM (1997) Perception of neighbouring plants by rhizomes and roots: morphological manifestations of a clonal plant. Can J Bot 75:2146–2157

    Article  Google Scholar 

  • Hutchings MJ (1997) Resource allocation patterns in clonal herbs and their consequences for growth. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic, California, pp 161–186

    Google Scholar 

  • Hutchings MJ, De Kroon H (1994) Foraging in plants, the role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238

    Article  Google Scholar 

  • Jackson RB, Caldwell MM (1989) The timing and degree of root proliferation in fertile soil microsites for three cold desert perennials. Oecologia 81:149–153

    Google Scholar 

  • Jaffe MJ, Shotwell M (1980) Physiological studies on pea tendrils. XI. Storage of tactile sensory information prior to the light activation effect. Physiol Plant 50:78–82

    Google Scholar 

  • Jennings DH, Trewavas AJ (1986) Plasticity in plants. Symp Soc Exptl Biol Med XL. Cambridge University Press, Cambridge

    Google Scholar 

  • Jones M, Harper JL (1987) The influence of neighbours on the growth of trees. I. The demography of buds in Betula pendula. Proc R Soc Lond Ser B Biol Sci 232:1–18

    Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage. A dialogue between genes and synapses. Science 294:1030–1038

    Article  PubMed  CAS  Google Scholar 

  • Kelly CK (1992) Resource choice in Cuscuta europea. Proc Natl Acad Sci USA 89:12194–12197

    PubMed  CAS  Google Scholar 

  • Kelly CL (1990) Plant foraging: a marginal value model and coiling response in Cuscuta subinclusa. Ecology 71:1916–1925

    Google Scholar 

  • Kim M, Canio W, Keller S, Sinha N (2001) Developmental changes due to long distance movement of a homeo-box fusion transcript in tomato. Science 293:287–293

    Article  PubMed  CAS  Google Scholar 

  • Kuppers M (1994) Canopy gaps: competitive light interception and economic space filling. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York,pp 111–144

    Google Scholar 

  • La Cerra P (2003) The first law of psychology is the second law of thermodynamics: the energetic model of the mind and the generation of human psychological phenomena. Hum Nat Rev 3:440–447

    Google Scholar 

  • La Cerra P, Bingham R (1998) The adaptive nature of the human neuro-cognitive architecture: an alternative model. Proc Natl Acad Sci USA 95:11290–11294

    Article  PubMed  Google Scholar 

  • La Cerra P, Bingham R (2002) The origin of minds. Harmony Books, New York

    Google Scholar 

  • Laroche A, Geng XM, Singh J (1992) Differentiation of freezing tolerance and vernalisation responses in Cruciferae exposed to a low temperature. Plant Cell Environ 15:439–446

    Google Scholar 

  • Mac Donald SE, Leiffers VJ (1993) Rhizome plasticity and clonal foraging of Calamagrostis canadensis in response tot habitat heterogeneity. J Ecol 81:769–776

    Google Scholar 

  • Mahall BE, Callaway RM (1992) Root communication mechanism and intra-community distributions of two Mojave desert shrubs. Ecology 73:2145–2151

    Google Scholar 

  • Maina GG, Brown JS, Gersani M (2002) Intra-plant versus inter-plant competition in beans: avoidance resource matching or tragedy of the commons. Plant Ecol 160:235–247

    Article  Google Scholar 

  • Marx J (2004) Remembrance of Winter Past. Science 303, 1607

    Article  PubMed  CAS  Google Scholar 

  • Maslov S, Sneppen K (2002) Specificity and topology of protein networks. Science 296:910–913

    Article  PubMed  CAS  Google Scholar 

  • Massa GD, Gilroy S (2003) Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. Plant J 33:435–445

    Article  PubMed  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    PubMed  CAS  Google Scholar 

  • McConnaughay KDM, Bazzaz FA (1991) Is physical space a soil resource? Ecol 72:94–103

    Google Scholar 

  • McConnaughay KDM, Bazzaz FA (1992) The occupation and fragmentation of space: consequences of neighbouring shoots. Funct Ecol 6:711–718

    Google Scholar 

  • McNamara JM, Houston AJ (1996) State dependent life histories. Nature 380:215–220

    Article  PubMed  CAS  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Ann Rev Microbiol 55:165–199

    Article  CAS  Google Scholar 

  • Muth CC, Bazzaz FA (2002a) Tree seedling canopy responses to conflicting photosensory cues. Oecologia 132:197–204

    Article  Google Scholar 

  • Muth CC, Bazzaz FA (2002b) Tree canopy displacement at forest gap edges. Can J Forest Res 32:247–254

    Article  Google Scholar 

  • Muth CC, Bazzaz FA (2003) Tree canopy displacement and neighbourhood interactions. Can J Forest Res 33:1323–1330

    Article  Google Scholar 

  • Nakagaki T, Yamada H, Toth A (2000) Maze solving by an amoeboid organism. Nature 407:470

    Article  PubMed  CAS  Google Scholar 

  • Novoplansky A (1996) Hierarchy establishment among potentially similar buds. Plant Cell Environ 19:781–786

    Google Scholar 

  • Novoplansky A (2003) Ecological implications of the determination of branch hierarchies. New Phytol 160:111–118

    Article  Google Scholar 

  • Novoplansky A, Cohen D, Sachs T (1989) Ecological implications of correlative inhibition between plant shoots. Physiol Plant 77:136–140

    Google Scholar 

  • Novoplansky A, Cohen D, Sachs T (1990) How Portulaca seedlings avoid their neighbours. Oecologia 82:490–493

    Article  Google Scholar 

  • Okamoto M, Sakai T, Hayashi K (1987) Switching mechanism of a cyclic enzyme system: role as a chemical diode. Biosystems 21:1–11

    Article  PubMed  CAS  Google Scholar 

  • Palladin PI (1918) Plant Physiology. Blakiston Son and Co., Philadelphia

    Google Scholar 

  • Park S, Wolanin PM, Yuzbashyan EA, Silberzan P, Stock JB, Austin RH (2003a) Motion to form a quorum. Science 301:188

    Article  PubMed  CAS  Google Scholar 

  • Park S, Wolanin PM, Yuzbashyan EA, Lin H, Darnton NC, Stock JB, Silberzan P, Austin RH (2003b) Influence of topology on bacterial social interaction. Proc Natl Acad Sci USA 100:13910–13915

    Article  PubMed  CAS  Google Scholar 

  • Peak D, West JD, Messenger SM, Mott KA (2004) Evidence for complex collective dynamics and emergent-distributed computation in plants. Proc Natl Acad Sci USA 101:981–922

    Article  CAS  Google Scholar 

  • Pearcy RW, Chardin RL, Gross LJ, Mott KA (1994) Photosynthetic utilisation of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, New York,pp 175–209

    Google Scholar 

  • Perkel JM (2004) Validating the interactome. Scientist 18:19–22

    Google Scholar 

  • Ravasz E, Somera AL, Mongru DA, Oltvai ZN, Barabasi AL (2002) Hierarchical organisation of modularity in metabolic networks. Science 297:1551–1555

    Article  PubMed  CAS  Google Scholar 

  • Robertson GP, Gross KL (1994) Assessing the heterogeneity of below ground resources: quantifying pattern and scale. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants. Academic, London, pp 237–253

    Google Scholar 

  • Sachs T, Novoplansky A Cohen D (1993) Plants as competing populations of redundant organs. Plant Cell Environ 16:765–770

    Google Scholar 

  • Schenk HJ Callaway RM Mahall BE (1999) Spatial root segregation: are plants territorial? Adv Ecol Res 28:145–180

    CAS  Google Scholar 

  • Schieving F, Poorter H (1999) Carbon gain in a multi-species canopy: the role of specific leaf area and photosynthetic nitrogen use efficiency in the tragedy of the commons. New Phytol 143:201–211

    Article  Google Scholar 

  • Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Schull J (1990) Are species intelligent? Behav Brain Sci 13:63–108

    Google Scholar 

  • Seeley TD (1995) The Wisdom of the hive. The social physiology of honey bee colonies. Harvard University Press, Harvard, Cambridge, MA

    Google Scholar 

  • Seeley TD, Leven RA (1987) A colony of mind. The beehive as thinking machine. Sciences 27:38–43

    Google Scholar 

  • Silvertown J, Gordon GM (1989) A framework for plant behavior. Ann Rev Ecol Syst 20:349–366

    Article  Google Scholar 

  • Slade AJ, Hutchings MJ (1987) Clonal integration and plasticity in foraging behavior in Glechoma hederacea. J Ecol 75:1023–1036

    Google Scholar 

  • Stenhouse D (1974) The Evolution of intelligence-a general theory and some of its implications. George Allen and Unwin, London

    Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–541

    Article  PubMed  CAS  Google Scholar 

  • Taiz L, Zeiger E (1998) Plant physiology, 2nd edn. Sinauer Associates, Massachusetts

    Google Scholar 

  • Thaler DS (1994) The evolution of genetic intelligence. Science 264:1698–1699

    PubMed  Google Scholar 

  • Tremmel DC, Bazzaz FA (1993) How neighbour canopy architecture affects target plant performance. Ecology 74:2114–2124

    Google Scholar 

  • Tremmel DC, Bazzaz, FA (1995) Plant architecture and allocation in different neighbourhoods: implications for competitive success. Ecology 76:262–271

    Google Scholar 

  • Trewavas AJ (1986) Resource allocation under poor growth conditions. A major role for growth substances in plasticity. In: Jennings DH, Trewavas AJ (eds) Plasticity in plants. Symp Soc Exp Biol Med XL. Company of Biologists, Cambridge, pp 31–77

    Google Scholar 

  • Trewavas AJ (1992) Growth substances in context: a decade of sensitivity. Biochem Soc Trans 20:102–108

    PubMed  CAS  Google Scholar 

  • Trewavas AJ (1998) The importance of individuality. In: Loerner HR (ed) Plant responses to environmental stresses. Dekker, New York,pp 27–43

    Google Scholar 

  • Trewavas AJ (1999) Le calcium c'est la vie; calcium makes waves. Plant Physiol 120:1–6

    Article  PubMed  CAS  Google Scholar 

  • Trewavas AJ (2000) Signal perception and transduction. In: Buchanan BBB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Maryland, pp 930–988

    Google Scholar 

  • Trewavas AJ (2003) Aspects of plant intelligence. Ann Bot 92:1–20

    Article  PubMed  CAS  Google Scholar 

  • Trewavas AJ (2004) Aspects of plant intelligence: an answer to Firn. Ann Bot 93:353–357

    Article  PubMed  Google Scholar 

  • Trewavas AJ (2005) Green plants as intelligent organisms. In: Conway-Morris S (ed) Convergence in ewvolution-some wider implications (in press)

  • Trewavas AJ, Malho R (1997) Signal perception and transduction: the origin of the phenotype. Plant Cell 9:1181–1195

    Article  PubMed  CAS  Google Scholar 

  • Turkington R, Aarsen LW (1984) Local scale differentiation as a result of competitive interactions. In: Dirzo R, Sarukhan J (eds) Pespectives on plant population ecology. Sinauer Associates, Massachusetts, pp 107–128

    Google Scholar 

  • Turkington R, Klein E (1991) Integration among ramets of Trifolium repens. Can J Bot 69:226–228

    Google Scholar 

  • Turkington R, Sackville Hamilton R, Gliddon C (1991) Within-population variation in localised and integrated responses of Trifolium repens to biotically patchy environments. Oecologia 86:183–192

    Article  Google Scholar 

  • Verdus MC, Thellier M, Ripoli C (1997) Storage of environmental signals in flax; their morphogenetic effect as enabled by a transient depletion of calcium. Plant J 12:1399–1410

    Article  CAS  Google Scholar 

  • Vertosick FT, Kelly RH (1991) The immune system as a neural network: a multi-epitope approach. J Theor Biol 150:225–237

    PubMed  CAS  Google Scholar 

  • Vertosick FT (2002) The Genius within. Discovering the intelligence of every living thing. Harcourt, New York

    Google Scholar 

  • Von Sachs J (1879) Lectures on the physiology of plants. (Translated by Marshall H, 1887). Oxford at the Clarendon Press, Oxford, UK

    Google Scholar 

  • Waddington CH (1957) The strategy of the genes. Jonathan Cape, London

    Google Scholar 

  • Warwick K (2001) The quest for intelligence. Judy Piatkus, London

    Google Scholar 

  • White J (1984) Plant metamerism. In: Dirzo R, Sarukhan J (eds) Perspectives on plant population ecology. Sinauer Associates, Massachusetts, pp 15–48

    Google Scholar 

  • Wijesinghe DK, Hutchings MJ (1999) The effects of environmental heterogeneity on the performance of Glechoma hederacea: the interactions between patch contrast and patch scale. J Ecol 87:860–872

    Article  Google Scholar 

  • Yamada T, Okuda T, Abdullah, M, Awang, M, Furukawa A (2000) The leaf development process and its significance for reducing self-shading of a tropical pioneer tree species. Oecologia 125:476–482

    Article  Google Scholar 

  • Zhong GY, Dvorak J (1995) Chromosomal control of the tolerance of gradually and suddenly-imposed salt stress in the Lophopyrum elongatum and wheat genomes. Theor Appl Gen 90:229–236

    Article  Google Scholar 

Download references

Author information

Affiliations

  1. Institute of Cell and Molecular Biology, University of Edinburgh, Kings Buildings, Edinburgh, EH9 3JH, UK

    Anthony Trewavas

Authors
  1. Anthony Trewavas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony Trewavas.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Trewavas, A. Plant intelligence. Naturwissenschaften 92, 401–413 (2005). https://doi.org/10.1007/s00114-005-0014-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-005-0014-9

Keywords

  • Intelligent Behavior
  • Plant Behavior
  • Palladin
  • Relative Residence Time
  • Animal Intelligence