Plant Signaling & Behavior

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Extended cognition in plants: is it possible?

André Geremia Parise, Monica Gagliano & Gustavo Maia Souza

To cite this article: André Geremia Parise, Monica Gagliano & Gustavo Maia Souza (2020)
Extended cognition in plants: is it possible?, Plant Signaling & Behavior, 15:2, 1710661, DOI:
10.1080/15592324.2019.1710661

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PLANT SIGNALING & BEHAVIOR
2020, VOL. 15, NO. 2, e1710661 (5 pages)
https://doi.org/10.1080/15592324.2019.1710661

CONCEPT PAPER

Extended cognition in plants: is it possible?

André Geremia Parisea, Monica Gaglianob,c, and Gustavo Maia Souza a

a
Laboratory of Plant Cognition and Electrophysiology (LACEV), Department of Botany, Institute of Biology, Federal University of Pelotas, Pelotas,
Brazil; bBiological Intelligence (BI) Laboratory, School of Life and Environmental Sciences, The University of Sydney, Sydney, Australia; cSydney
Environment Institute (SEI), The University of Sydney, Sydney, Australia

ABSTRACT ARTICLE HISTORY

Plants do not possess brains or neurons. However, they present astonishingly complex behaviors such as Received 23 October 2019
information acquisition, memory, learning, decision making, etc., which helps these sessile organisms deal Revised 22 December 2019
with their ever-changing environments. As a consequence, they have been proposed to be cognitive and Accepted 24 December 2019
intelligent, an idea which is becoming increasingly accepted. However, how plant cognition could operate KEYWORDS
without a nervous central system remains poorly understood and new insights on this topic are urgently Extended cognition; plant
needed. According to the Extended Cognition hypothesis, cognition may also occur beyond the limits of the behavior; mycorrhizae;
body, encompassing objects from the environment. This was shown possible in humans and spiders, who rhizosphere; plant
actively manipulate their external environment to extend their cognitive capacity. Here, we propose that intelligence; foraging
extended cognition may also be found in plants and could partly explain the complexity of plant behavior.
We suggest that plants can extend their cognitive abilities to the environment they manipulate through the
root influence zone and the mycorrhizal fungi that associate with them. The possibility of a cognitive process
involving organisms from different kingdoms is exciting and worthwhile exploring as it may provide key
insights into the origin and evolution of cognition.

The boundaries of cognition: an exciting field of about ascribing cognitive capacities to animals with tiny
debate brains such as insects, and difficulties with the idea of cogni-
tion in organisms such as plants that lack these anatomical
All organisms have evolved ways of sensing and adaptively
structures entirely. Yet, despite their miniature brains, insects
interacting with the world. In wild, real-world environments,
display a complex behavioral repertoire mediated by sophis-
where circumstances are variable, and survival is uncertain,
ticated cognitive abilities.3 And with no brain at all, plants too
organisms do not simply react to the external impingements
exhibit a wide range of exquisite behaviors,4 which has
but actively explore their environment and modify their beha-
recently revealed unsuspected cognitive capacities in these
vior in flexible, context-sensitive ways related to fitness com-
non-neural organisms (e.g. Gagliano et al.5,6). The new experi-
ponents such as growth, reproduction and ultimately,
mental evidence casts doubts on the validity of the classical
survival. Organisms must interpret the environment to fit
view of cognition centered on the brain, and instead, more
well into it. The choices, decisions and actions they make to
closely aligns with theoretical post-cognitivist models that
deal with the varying demands and challenges they face reveal
have proposed alternative ways of exploring cognitive pro-
their underlying intelligence.1 Processes like remembering,
cesses and their limits beyond neural bounds.7–12
making associations, perceiving, learning, solving problems,
From a post-cognitivist perspective, cognition takes place in
deciding and acting that bring about such intelligent behavior
the context of a real-world environment and inherently involves
define their cognition.2
perception and action. The process of perception-action occurs
Much has been discussed about the limits and bounds of
in the context of environmental contingencies, and the resulting
cognition across taxa. Such discussions are shaped by how we
behavior can be more or less affected by external stimuli.13,14 The
define ‘cognition’ and what we count as ‘cognitive’. The clas-
extent to which the environment influences the organism
sical view of cognition (or cognitivism) assumes that a large
depends on the organism’s capacity to sense the environment
brain and a complex neural system are necessary to support
and the organism’s level of autonomy from it (i.e. an organism’s
cognitive capacities. The core idea is that cognition pertains to
capacity of keeping its auto-organization despite the environ-
the specific properties of the brain. The brain is treated as the
mental fluctuations that act on it; Souza et al.15, Souza and
information-processor that operates by receiving data from
Lüttge16). From this perspective, cognition is not exclusively
the environment in the form of symbolic inputs that it manip-
confined to an organism’s brain or the nervous system. Rather,
ulates into internal representations to produce a relevant out-
it can be distributed, when the cognitive capacity required for
put in the form of different behaviors and experiences. Given
completing a task is spread among many individuals of the same
such premise, it is unsurprising that we have reservations
species (e.g. the ‘hive mind’ of ants in a colony or the crew in an

CONTACT André Geremia Parise [email protected] Laboratory of Plant Cognition and Electrophysiology (LACEV), Department of Botany, Institute of
Biology, Federal University of Pelotas, Pelotas, Brazil
© 2019 Taylor & Francis Group, LLC
e1710661-2 A. G. PARISE ET AL.

aircraft cockpit); embodied, when some cognitive control is B and vice versa. To further elucidate the mutual manipulability
devolved to parts of the body other than the central brain, thus criterion and clarify how it is already used – although not expli-
spanning the cognitive process to all the body of the organism citly – in neurobiological sciences, Kaplan29 referred to experi-
(e.g. the multifaceted camouflage of the common cuttlefish and ments performed with monkeys by Talbot et al.32 They found that
complex bending movements of the tentacle performed by the a mechanical vibration applied to the hand of a monkey activated
common octopus); and even extended, where physical objects in a specific region of their brains invoking action potentials at
the world form part of the cognitive system of the animal that a certain frequency. In a subsequent experiment performed
built or manipulates them (e.g. nest-building weaver ants and years later, Romo et al.33 demonstrated that by electrically stimu-
web-building garden spiders). For a review of these ‘species’ of lating this same brain area with the same frequency, monkeys
cognition, see Cheng9 and Lavoie et al.17 bearing in mind that reacted as if they were being stimulated on the hand. Due to the
the overall classification of cognitive ‘species’ provides us with an mutual manipulability of the cognitive system’s presumed ele-
initial context in which to specifically design and interpret ments, its causal relationship was established.29 This example
experimental work and that these ‘species’ are not mutually does not specifically describe a case of extended cognition, but
exclusive (i.e. they can and do co-occur). While a post- rather a case of embodied cognition; however, it is important
cognitivist take on cognition implicitly includes non-neuronal because it showcases how mutual manipulability can be applied
organisms (and have received extensive philosophical considera- as a good empirical approach for defining the bounds of
tion; see Calvo & Keijzer18,19 and Segundo-Ortin and Calvo20, a cognitive system (be it extended or not).
for specific plant examples), existing experimental studies have It is important to distinguish between genuine components of
still solely focused on organisms with a brain and neural system. an extended cognitive system from what Kaplan29 called “causal
Hence, we need to explicitly include brainless organisms such as background conditions”. Sometimes, components of a system are
plants in our experimental investigations of cognition. Here, we related by simple causality and are not part of the cognitive
will consider the possibility of extended cognition in plants. process. For example, it is widely known that oxygen is required
for normal brain activity. As a person is engaged in a cognitive
task, certain areas of the brain will engage in greater activity and in
The extended cognition from humans to spiders
turn, this increased activity might increase the consumption of
Over two decades ago, Clark and Chalmers21 put forward the idea oxygen for respiration. On the other hand, if the supply of oxygen
that cognition extends beyond the seeming physical boundary of to the brain is interrupted, cognitive processes are compromised.
the organism (i.e. embodied) into its environment (i.e. embedded) It would be tempting to say that the mutual manipulability criter-
and involves objects that are not part of the body. This is known as ion is satisfied here; oxygen would be considered part of the
the Extended Cognition hypothesis. According to this hypothesis, cognitive process and human cognition would extend to the
the environment plays an active role in driving the cognitive oxygen surrounding us. However, a person engaged in
processes, which are not confined to the central nervous system a cognitive task does not alter the concentration of oxygen in
or the body, and involve the manipulation of the environment by the immediate surrounding. Under this scenario A affects B, but
the organism to enhance its cognitive abilities. For example, in B does not affect A. Oxygen will always be oxygen and, unless this
humans, the simple use of pen and paper to write a note or person is closed in a sealed room, it will be present in more or less
“sketch” a thought represents a way of extending our ability to the same atmospheric concentration. Besides, enhancing the
remember beyond the brain, making manageable what may amount of oxygen in the brain (by increasing its concentration
otherwise be information overload. More poignantly, our depen- in the air) will not make the person spontaneously engage in
dence on computers and smartphones speaks volumes about how a cognitive task or activate the same brain areas. So, oxygen is
much we offload our cognitive capacity to external devices.22,23 a mere causal background condition, a necessary substrate for the
The idea that cognition may not be restricted to the brain but cognitive process as is gravity for walking. Again, if we change
extends beyond the boundaries of the physical body was received gravity, we change our ability to walk on land. Yet (and fortu-
both favorably and with criticism. The critics, who espoused the nately), walking does not affect the Earth’s gravity. This is another
idea that cognition begins and ends in the brain, were concerned example of a causal background condition that enables walking.
by the fact that it seemed particularly difficult to empirically test Extended cognition is different from embedded cognition in
and demonstrate that a given process is an inextricable part of the the sense that the latter emerges from the interaction of an
observed cognitive system.24–28 Kaplan29 proposed to resolve the organism with its environment, but the cognitive process remains
issue by using the mutual manipulability criterion.30,31 According firmly within the body, despite the essential role of the environ-
to this criterion, if intervening in one of the components of ment in the process.12 For extended cognition, the cognitive
a mechanism alters the mechanism’s overall behavior, and if by process occurs within and beyond the physical body and includes
altering the whole mechanism the behavior of the component is the external objects that are manipulated by the organism.
also changed, then both are part of the same mechanism.31 The idea of extended cognition was received favorably by
According to Kaplan29 if there is a relationship of mutual manip- evolutionary biologists who worked on niche construction
ulability between the putative components of the cognitive system, theory,34–36 especially in the context of spider ecology.34,37
then we can demarcate its bounds. For example, suppose that Spiders present a vast array of complex behaviors and cogni-
A and B are suspected to be part of the same cognitive process, tive abilities that defy the relationship between brain size and
where A is the wider phenomenon under study (cognition) and behavioral complexity, challenging the hypothesis that com-
B the external object that is supposed to be part of this phenom- plex cognitive skills have a straightforward relation with larger
enon. Manipulation of A should causally affect the behavior of brains.38 In their review article, Japyassú and Laland34 argued
 PLANT SIGNALING & BEHAVIOR e1710661-3

that spiders extend their cognitive capacities to the webs they the cognitive state of the plant alters one of these components
spin. They proposed that by transferring part of the informa- and the manipulation of the component alters the plant’s
tion processing to their webs, spiders simultaneously avoid cognitive state, then according to the mutual manipulability
compromising their cognitive abilities and overloading their criterion, both are part of the same system demarcated via an
small brains. In effect, the spider plus its web would constitute extended cognition process. For example, environmental tem-
the cognitive system. In support of their hypothesis, Japyassú perature directly affects plant cognition, for changes in tem-
and Laland34 offered several cases in which spider relations perature can speed up or slow down metabolic processes and,
with their webs met the mutual manipulability criterion. For by extension, the plant’s capacity of processing and respond-
example, the web of many spider species serves as a ‘filter’ for ing to the stimuli perceived in the environment. In principle,
which information will reach the spider. This information a plant’s cognitive activity can alter the temperature immedi-
reaches the spider codified in the form of vibrations of the ately around the plant via the opening and closing of the
threads caused by external agents such as wind or some stomata (a process which requires exquisite computing abil-
captured insect.37,39 By pulling more strongly the threads of ities; Peak et al.44, Merilo et al.45) and affect transpiration
a particular area of the web, the spider can focus its attention rates. However, these temperature alterations will not change
in the desired web section, enhancing its success in catching the transfer of thermal energy from the environment to the
its prey. Normally, the spider’s attention is directed toward plant. The mutual manipulability criterion is not properly met
the most profitable web areas. By artificially manipulating the here: heat is a causal background condition and not part of
tension on the web threads, one can alter the foraging beha- the cognitive process. Let’s now consider cases where the
vior of the spider, inducing it to pay attention to other areas mutual manipulability criterion for extended cognitive pro-
of the web, even though these areas have previously been cesses in plants might be satisfied.
unfruitful.39,40 The spider responses to the stimuli and its Plants could extend their cognitive processes and amplify the
information processing are intimately conditioned to web perception of the underground world beyond the physical limit
tension, and not only to its central nervous system,34 demon- of their roots by actively modifying the rhizosphere and the roots
strating that the manipulation of the spider’s web or its influence zone. For example, the perception of obstacles in the
central nervous system modifies the cognitive capacities of soil is related to the accumulation of allelopathic exudates
the spider and its understanding of the world. These findings between the obstacle and the root.46 This causes root growth to
also demonstrated that the idea of extended cognition can be be inhibited in the direction in which the exudates are being
applied not only to humans but also other organisms, espe- accumulated. Falik et al.46 found that the experimental removal
cially those who build niches for themselves. Here we discuss of the exudates from the substrate prevented the plant from
the possibility that brainless organisms like plants may also perceiving the obstacle and made its roots grow toward it as if
extend their cognition beyond their bodies. not present. The relationship between a plant and its exudates
meets the mutual manipulability criterion affecting plant cogni-
tion, and like the spider with its web, the plant plus its exudates
Extended cognition: extending it to plants
constitute the cognitive system.
Unlike most animals that can wander in search of food and The cognition of plants could be extended beyond this first
flee when perceiving threat, plants are sessile organisms that example to the associated bacterial community of the roots.
live inextricably grounded in their environment. Like their Plants actively manipulate the microbiome in the rhizosphere
animal counterparts, plants have evolved very refined and for their own sake. For example, Huang et al.47 have demon-
sophisticated sensory abilities to constantly perceive and strated that Arabidopsis has specific pathways for synthesizing
monitor their surroundings41,42 and perform astonishingly triterpenes that modulate the community of bacteria that lives in
complex behaviors without a brain or any other centralized its rhizosphere, which creates an Arabidopsis-specific bacterial
organ. How is this possible? Might it be conceivable that like community. However, the abundance and diversity of this com-
spiders, plants “offload” (see Risko & Gilbert43 on cognitive munity can be altered by the plant through the many different
offloading) at least part of their cognitive process to the substances exudated by the roots, and the composition of the
environment by extending their cognition beyond their microbial community can encode memories in the soil, outside
bodies? If so, how could a plant extend its cognition? We the plant’s body. In a study conducted by Yuan et al.48 five
propose primarily two ways in which a plant may do this: by generations of Arabidopsis infected by Pseudomonas syringae
means of their root exudates and by means of the micro- pv tomato were grown in the same pot, and the plants have
organisms that live associated with the roots. altered the substrate microbiota by secreting several different
Before presenting examples of studies that seem to satisfy substances that modulated the bacterial community. When the
the mutual manipulability criterion for extended cognitive fifth Arabidopsis was removed from the pot and a sixth
processes in plants, it is important to make the clear distinc- Arabidopsis was planted in this same soil, the plant became
tion between the plant’s extended cognition from simple significantly more resistant to this pathogen.
causal background conditions. The mutual manipulability Plants could also extend their cognitive processes via their
criterion can help us make this distinction clear. Firstly, we association with the mycorrhizal fungi they live with. During
consider the wider phenomenon we intend to demarcate, the root colonization process, fungi penetrate the plant’s roots
namely plant cognition. Then, we consider the components and establish an interface where many different molecules and
in the environment that could be part of the plant’s cognitive signals are constantly exchanged.49 The fungi enormously
system because the plant can manipulate them in some way. If amplify the roots’ absorbing area and help the plants in the
e1710661-4 A. G. PARISE ET AL.

uptake of water and nutrients, such as phosphorus. In return, Acknowledgments

plants repay the fungi with photoassimilates.50 Through the
The authors thank the LACEV’s members for enthusiastic and
association with mycorrhizae, plants can amplify their own insightful discussions, five reviewers for their constructive comments
perception and perceive things that are out of their reach. and M Depczynski for providing feedback and proofreading the final draft.
Based on what the mycorrhizae perceive and absorb in
a particular region of the soil, for example, a plant could
make choices about the growth direction of its roots and Disclosure of potential conflicts of interest
predict nutrient patches, water, or even forthcoming stress The authors declare that the research was conducted in the absence of
well before the roots get close enough to detect these any commercial or financial relationships that could be construed as
resources or cues themselves. Therefore, the fungal network a potential conflict of interest.
could extend the plant’s perception of the environment and
facilitate cognitive processes such as communication, learning
Funding
and memory in plants.50
Clearly, not all responses and outcomes are the result of, or AGP and GMS are granted with a scholarship from the Conselho
require, cognition. Hence, for this plant plus fungus to be con- Nacional de Desenvolvimento Científico e Tecnológico (CNPq -
sidered a cognitive system, the cognitive processes involved must Brazil). GMS is a CNPq research fellow. MG is supported by the
Templeton World Charity Foundation (TWCF) under the Diverse
satisfy the mutual manipulability criterion. According to this Intelligences Initiative.
criterion, experiments designed to determine whether the fungus
represents a true extension of the plant’s cognitive system will
have to establish a two-way flow, where the fungus plays an ORCID
active role in driving the cognitive processes of the plant (e.g. Gustavo Maia Souza http://orcid.org/0000-0001-6754-4860
while locating nutrients in the soil or navigating a complex
environment) and at the same time, the manipulation of the
fungus by the plant enhances the plant’s cognitive abilities. To References
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