Abstract
Considering that plant intelligence is a not an exception, but the basic expression of the plasticity of the living world, we propose to investigate plant sensing and non-explicit cognitive skills of plants through a mesological prism. This could echo recent debates on plant sensitivity or felt states and open new perspectives on the cognitive capacities of brainless organisms. These questions will be addressed relatively to our very results in the cross-field of biosemiotics and mesological plasticity for the theoretical part, and of recent plant electrome studies related to perception, cognition, decision-making or attention-like processes for the experimental part. One tentative response could be that on-line cognition and non-explicit cognitive skills are relevant for plants (and non-neural organisms) not meeting the essential markers of animal or human sentience such as the ability to experience feelings, emotions, or subjectivity. For plants, however we should consider their own ecosystemic and active sensory-cognitive areas including phenotypic and epigenetic plasticity as well as their fine-tuned electromic pathways. Another response might be that only evolutionary biology and post-cognitivist transdisciplinary approaches involving both raw biological data and empirical or mesological considerations of the plant-milieu interface could permit us to apprehend the high and underestimated cognitive power underlying plant complex behaviors. Our objective will thus consist in determining how far these cognitive powers and/or cognitive abilities extend and what ways might have plants to access experience. Furthermore, we shall attempt to establish a new ecosensitive assessment of plant cognition considering the new form of plasticity we are describing on a mesological scale. . This would allow in the future to consider plants as essential medial structures at the plant-milieu interface and to redefine the boundaries of cognition thus putting an end to the circular debates about the deep nature of plant sentience, cognition or intelligent behaviors compared to animal and human.
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Abbreviations
- OLC:
-
On-line cognition
- OFC:
-
Off-line cognition
- NECS:
-
Non explicit cognitive skills
- CP:
-
Cognitive power
- NS:
-
Nervous system
- MP:
-
Mesological plasticity
- DMN:
-
Default mode network
- PC:
-
Plasticity complexes
References
Baciadonna L, Macri C, Giurfa M (2023) Associative learning: unmet criterion for plant sentience. Anim Sentience 478:1
Baluška F (2013) Long-distance systemic signaling and communication in plants, 1st edn. Springer, Berlin
Baluška F, Mancuso S (2009) Plants and animals: convergent evolution in action? In: Plant-environment interactions: from sensory plant biology to active plant behavior. Springer, Berlin
Baluška F, Yokawa K (2021) Anaesthetics and plants: from sensory systems to cognition-based adaptive behaviour. Protoplasma 258(2):449–454. https://doi.org/10.1007/s00709-020-01594-x
Animal Welfare. Animal Sentience, 2016.00
Berque A (2008) Ecumene - introduction to the study of human environments. Belin, Paris
Berque A (2014) Footprint Forms, Matrix Forms, East Asia, Franciscopolis Ed
Berque A (2017) What is mesology? Blog Mesologiques, Etude des milieux, Paris
Booth DA (2023) Back to the science from the words. Anim Sentience 33:9
Borghans L, Duckworth AL, Heckman JJ, Ter Weel B (2008) The economics and psychology of personality traits. J Hum Resour 43(4):972–1059
Brenner E, Stahlberg R, Mancuso S, Vivanco J, Baluška F, Van Volkenburgh E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11(8):413–419. https://doi.org/10.1016/j.tplants.2006.06.009
Brooks Pribac T (2021) Enter the animal: cross-species perspectives on grief and spirituality. Sydney University Press, Sydney
Broom DM (2014) Sentience and animal welfare. CABI, Wallingford
Broom DM (2022) Concepts and interrelationships of awareness, consciousness, sentience, and welfare. J Conscious Stud 29:1
Cabral EF, Pecora PC, Arce AIC, Tech ARB, Costa EJX (2011) The oscillatory bioelectrical signal from plants explained by a simulated electrical model and tested using Lempel-Ziv complexity. Comput Electron Agric 76:1–5
Calvo P, Keijzer F (2009) Cognition in plants. In: Baluska F (ed) Plant-environment interactions: from sensory plant biology to active plant behaviour. Springer, Berlin
Calvo GP, Keijzer F (2011) Plants: adaptive behavior, root-brains, and minimal cognition. Int Soc Adapt Behav 19(3):155–171. https://doi.org/10.1177/105971231140946
Cheng K (2018) Cognition beyond representation: varieties of situated cognition in animals. Comp Cogn Behav Rev 13:1–20. https://doi.org/10.3819/CCBR.2018.130001
Crump A, Browning H, Schnell A, Burn C, Birch J (2022) Sentience in decapod crustaceans: a general framework and review of the evidence. Anim Sentience 32:1
Colaço D (2022) Why studying plant cognition is valuable, even if plants aren’t cognitive. Synthese 200:453. https://doi.org/10.1007/s11229-022-03869-7
Damasio A (1999) The feeling of what happens: body and emotion in the making of consciousness. Harcourt Brace, New York
Damasio A (2021) Feeling & knowing - making minds conscious. Pantheon Books, New York
De Loof A (2016) The cell’s self-generated “electrome”: the biophysical essence of the immaterial dimension of Life? Commun Integr Biol 9(5):e1197446. https://doi.org/10.1080/19420889.2016.1197446
De Toledo GRA, Parise AG, Simmi FZ, Costa AVL, Senko LGS, Debono MW, Souza GM (2019) Plant electrome: the electrical dimension of plant life. Theoret Exp Plant Physiol. https://doi.org/10.1007/s40626-019-00145-x.0123456789
Debono MW (2005) Le concept de plasticité : un nouveau paradigme épistémologique. Dogma https://www.dogma.lu/txt/MWD-ConceptPlasticite.htm
Debono MW (2013a) Dynamic protoneural networks in plants: a new approach of spontaneous extracellular potential variations. Plant Signal Behav 8:e24207
Debono MW (2013b) Perceptive levels in plants: a transdisciplinary challenge in living organism’s plasticity. Transdiscipl J Eng Sci 4:21–39
Debono MW (2020) Electrome & cognition modes in plants: a transdisciplinary approach to the eco-sensitiveness of the world. Transdiscipl J Eng Sci 11:213–239. https://doi.org/10.22545/2020/00143
Debono MW (2021) Le concept épistémologique de plasticité : évolution et perspectives. Dogma Ed. 15
Debono MW (2022) Mesological plasticity as a new model to study plant evolution, interactive ecosystems & self-organized evolutionary processes in Self-Organization as a New Paradigm in Evolutionary Biology: From Theory to Applied Cases in the Tree of Life, (Dambricourt Malassé A ed), Springer-Nature, Switzerland, Series Ed. R.G. Delisle, Vol 5:253–290. https://doi.org/10.1007/978-3-031-04783-1_10
Debono MW, Bouteau F (1992) Spontaneous and evoked surface potentials in Kalanchoe tissues. Plant Physiol 11:107–117
Debono MW, Souza GM (2019) Plants as electromic plastic interfaces: a mesological approach. Prog Biophys Mol Biol 146:123–133. https://doi.org/10.1016/j.pbiomolbio.2019.02.007
Di X, Biswal BB (2014) Identifying the default mode network structure using dynamic causal modeling on resting-state functional magnetic resonance imaging. Neuroimage 86:53–59. https://doi.org/10.1016/j.neuroimage.2013.07.071
Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257. https://doi.org/10.1111/j.1365-3040.2006.01614.x
Gagliano M, Mancuso S, Robert D (2012) Towards understanding plant bioacoustics. Trends Plant Sci 17(6):323–325
Gagliano M, Renton M, Depczynski M, Mancuso S (2014) Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63–72. https://doi.org/10.1007/s00442-013-2873-7
Gagliano M, Vyazovskiy VV, Borbély AA, Grimonprez M, Depczynski M (2016) Learning by association in plants. Sci Rep 6(38427):1–9. https://doi.org/10.1038/srep38427
Gardner B (2015) A review and analysis of the use of ‘habit’ in understanding, predicting and influencing health-related behavior. Health Psychol Rev 9:277–295
Gibson JJ (1979) The theory of affordances. In: Gibson JJ (ed) The ecological approach to visual perception. Houghton Mifflin, Boston
Gibson EJ, Pick AD (2000) Perceptual learning and development: an ecological approach to perceptual learning and development. Oxford University Press, Oxford
Gimenez VMM, Pauletti PM, Silva ACS, Costa EJX (2021) Bioelectrical pattern discrimination of Miconia plants by spectral analysis and machine learning. Theor Exp Plant Physiol 33:329–342
Gorzelak MA, Asay AK, Pickles BJ, Simard SW (2015) Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants. 7:050. https://doi.org/10.1093/aobpla/plv050
Jacobson A, Yang D, Vella M et al (2021) The intestinal neuro-immune axis: crosstalk between neurons, immune cells, and microbes. Mucosal Immunol 14:555–565. https://doi.org/10.1038/s41385-020-00368-1
Klein C, Barron B (2016) Insects have the capacity for subjective experience. Anim Sentience 9:1. https://doi.org/10.51291/2377-7478.1113
Kull K (2000) An introduction to phytosemiotics: semiotic botany and vegetative sign systems. Sign Syst Stud 28:326–350. https://doi.org/10.12697/SSS.2000.28.18
Kull K (2020) Jakob von Uexküll and the study of primary meaning-making. In: Michelini F, Köchy K eds Jakob von Uexküll and philosophy: life, environments, anthropology
Lee J (2023) What is cognitive about ‘plant cognition’? biol philos 38(3):1–21
Margulis L, Symbiogenesis, (2009) Hommage to Darwin: a debate on evolution. Balliol College, Oxford
Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluška F, Arecchi FT, Mancuso S (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci 106(10):4048–4053. https://doi.org/10.1073/pnas.0804640106
Marder M (2013) Plant intelligence and attention. Plant Signal Behav 8:e23902
Mediano P, Trewavas A, Calvo P (2021) Information and integration in plants: towards a quantitative search for plant sentience. J Conscious Sci 28:1
Miguel-Tomé S, Llinás RR (2021) Broadening the definition of a nervous system to better understand the evolution of plants and animals. Plant Signal Behav 16:10. https://doi.org/10.1080/15592324.2021.1927562
Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature 500:422–426
Nguyen CT, Kurenda A, Stolz S, Chetelat A, Farmer EE (2018) Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc Natl Acad Sci USA 115:10178–10183
Olkowicz S, Kocourek M, Lučan RK, Němec P (2016) Birds have primate-like numbers of neurons in the forebrain. Proc Natl Acad Sci USA 113(26):7255–7260. https://doi.org/10.1073/pnas.1517131113
Palfalvi G, Hackl T, Terhoeven N et al (2020) Genomes of the venus flytrap and close relatives unveil the roots of plant carnivory. Curr Biol 30(12):2312–2320. https://doi.org/10.1016/j.cub.2020.04.051
Panksepp J (1998) Affective neuroscience: the foundations of human and animal emotions. Oxford University Press, Oxford
Pereira DR, Papa JP, Saraiva GFR, Souza GM (2018) Automatic classification of plant electrophysiological responses to environmental stimuli using machine learning and interval arithmetic. Comput Electron Agric 145:35–42
Procko C, Murthy S, Keenan WT, Mousavi SAR, Dabi T, Coombs A, Procko E, Baird L, Patapoutian A, Chory, (2021) Stretch-activated ion channels identified in the touch-sensitive structures of carnivorous Droseraceae plants. Elife 10:64250. https://doi.org/10.7554/eLife.64250
Rudolph S, Badura A, Lutzu S, Pathak SS, Thieme A, Verpeut JL, Wagner MJ, Yang YM, Fioravante D (2023) Cognitive-affective functions of the cerebellum. J Neurosci 43(45):7554–7564. https://doi.org/10.1523/JNEUROSCI.1451-23.2023
Russo A, Pollastri S, Ruocco M, Monti MM, Loreto F (2022) Volatile organic compounds in the interaction between plants and beneficial microorganisms. J Plant Interact 17(1):840
Parise AG, de Carvahlo Oliveira TF, Debono MW and Souza GM (2023) The electrome of a parasitic plant in a putative state of attention increases the energy of low band frequency waves: a comparative study with neural systems 12(10):2005. https://doi.org/10.3390/plants12102005
Parise AG, Gagliano M, Souza GM (2020) Extended cognition in plants: is it possible? Plant Signal Behav 15(2):1710661. https://doi.org/10.1080/15592324.2019.1710661
Parise AG, de Toledo GRA, Oliveira TFC, Souza GM, Castiello U, Gagliano M, Marder M (2022) Do plants pay attention? A possible phenomenological-empirical approach. Prog Biophys Mol Biol 173:11–23. https://doi.org/10.1016/j.pbiomolbio.2022.05.008
Pessoa L (2023) What can plant science learn from animal nervous systems? Anim Sentience 33:6
Saraiva GRF, Ferreira AS, Souza GM (2017) Osmotic stress decreases complexity underlying the electrophysiological dynamic in soybean. Plant Biol 19(5):702–708. https://doi.org/10.1111/plb.12576
Schneider HM (2022) Characterization, costs, cues and future perspectives of phenotypic plasticity. Ann Bot 130(2):131–148
Segundo-Ortin M, Calvo P (2023) Plant sentience? Between romanticism and denial: science. Anim Sentience 33:1
Simmi F, Dallagnol L, Ferreira A, Pereira D, Souza G (2020) Electrome alterations in a plant-pathogen system: toward early diagnosis. Bioelectrochemistry 133:107493
Sims R, Yilmaz Ö (2023) Stigmergic coordination and minimal cognition in plants. Anim Sentience 33:1
Souza GM, de Toledo GRA, Parise AG, Costa AVL, Reissig GN, Oliveira TFC and Debono MW (2023) Plants as electromic plastic interfaces, 6th Symposium on Plant Signaling & Behavior June 18–22, Seattle, USA https://psb2023.org
Souza GM, de Toledo GRA, Saraiva FR (2018) Towards systemic view for plant learning: ecophysiological perspective. In: Baluška F, Gagliano M, Witzany G (eds) Memory and learning in plants. Springer, Cham
Souza GM, Ferreira AS, Saraiva GFR, Toledo GRA (2017) Plant “electrome” can be pushed toward a self-organized critical state by external cues: evidence from a study with soybean seedlings subject to different environmental conditions. Plant Signal Behav 12:e1290040. https://doi.org/10.1080/15592324.2017.1290040
Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity-complexity-diversity in eco-physiology. In: Lüttge U, Beyschlag W (eds) Progress in botany, vol 76. Springer, Cham, pp 211–239
Struik PC (2023) Plants detect and adapt, but do not feel. Anim Sentience 33:3
Thompson E (2010) “The enactive approach” In Mind in life: Biology, phenomenology, and the sciences of mind. Harvard University Press, Oxford
Trewavas A (2016) Intelligence, cognition, and language of green plants. Front Psychol 7:588. https://doi.org/10.3389/fpsyg.2016.00588
Trewavas A (2017) The foundations of plant intelligence. Interface Focus 7(3):20160098. https://doi.org/10.1098/rsfs.2016.0098
Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361(6407):1112–1115
von Uexküll J (1926) Theoretical biology. Harcourt, Brace & Co, New York
von Uexküll J (2010) A Foray into the worlds of animals and humans: with a theory of Meaning, translated by Joseph D. O’Neil. University of Minnesota Press, Minneapolis
Varela FJ, Thompson E, Rosch E (1992) The embodied mind: Cognitive science and human experience. MIT Press, New York
Volkov AG (2006) Plant electrophysiology. Springer, Berlin
Wang Q, Guerra S, Bonato B, Simonetti V, Bulgheroni M and Castiello U (2023) Decision-making underlying support-searching in pea plants. PrePrints.org https://doi.org/10.20944/preprints202303.0022.v1
Wang J, Wu D, Wang Y, Xie D (2019) Jasmonate action in plant defense against insects. J Exp Bot 70(13):3391–3400
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Debono, MW. The cognitive power of plants: from mesological plasticity to non-explicit cognitive skills. Theor. Exp. Plant Physiol. (2024). https://doi.org/10.1007/s40626-024-00332-5
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DOI: https://doi.org/10.1007/s40626-024-00332-5