What is Intelligence?
Charles Darwin was the first to fully scientifically describe a unique and incredibly plastic organism which possessed many more than the five basic senses, and which could rapidly and specifically respond to a diverse array of stimuli and to communicate with itself, it’s kin and its enemies. More amazingly, this organism was capable of regenerating any part of its body and could survive attacks which lead to almost complete destruction of its organs and tissues. Though this sounds like some sort of alien or super-engineered organism, it is in fact all around us, and something we are all familiar with, a plant. Although we often consider plants to be immobile, inanimate objects, plants are in fact intelligent beings with an incredible capacity to sense their environment, process complex signals, evaluate risk and reward and make choices based on current and future needs. The concept of plant intelligence was widely disputed when it was first presented by Charles Darwin and his son Francis Darwin in the late 1800’s – early 1900’s and while an increasing body of evidence is growing demonstrating the existence of plant intelligence, controversy still exists within the plant research community (Darwin, 1880). This divide comes down to an apparently simple, but extremely complex question, what is intelligence and what requirements must be met? It is further complicated by the innate human bias which is always associated with this type of discourse. Proponents of plant intelligence or plant neurobiology (a synonymous term utilized by researchers in the field) are quick to point out that they are not saying that plants have brains, or that plants have intelligence of the same kind of animals, the difficulty lies in our ability as humans to describe such contexts without the use of analogies, and comparisons to the system with which we are most familiar, ourselves. Opponents of this field, point out that plants do not posses a brain and are not conscious beings. It is therefore necessary, in any discussion of this topic to first determine what exactly defines “intelligence”.
Intelligence has been defined as “the ability to acquire and apply knowledge and skills”, “the ability to learn or understand things or to deal with new or difficult situations, “the skilled use of reason” and “the ability to apply knowledge to manipulate one’s environment or to think abstractly as measured by objective criteria (tests)”. In the scientific literature definitions rely heavily on the ability of an organism to solve problems and is assessed and defined in the context of behaviour. In this context the intelligence is defined as a complex adaptive behaviour that maximizes fitness, another term given us by Darwin. Though not all behaviour is intelligent, those contributing to the existence of intelligence include: detailed sensory processing, learning, memory, choice, self recognition, and the ability to predict and adapt based on future resource and nutrition requirements (resource allocation and predictive modelling)(Trewavas, 2005).
Can Plants See, Taste, Smell, Feel, Hear?
Plants have demonstrated all these traits through various behaviours and adaptations, and in fact the traditional five senses can be assigned to plant behaviours as well as an estimated fifteen or more additional senses, or as they are referred to in the plant science world, tropisms, including typical tropisms such as gravi- (gravity), thermo- (temperature) and hydro- (water) tropisms, but also integrate such diverse information as electric fields, magnetic fields and the same gravity forces induced by the movement of the Earth around the sun and the moon around Earth which control ocean tides (lunisolar tidal acceleration) (Fig 1; Barlow et al., 2013). In fact, plants sense and evaluate many diverse stimuli, including abiotic (non-living, e.g. humidity, temperature) and biotic (living; e.g. pathogens) stimuli, and can assess and prioritize responses depending on the level of importance, based on current and future needs and demands of the plant. These responses can involve reactions at the biochemical level and the balance of individual growth regulating compounds such as the aspirin relative salicyclic acid and jasmonic acid. The former is important in response to pathogen challenge, while the latter mediates herbivore attack and a proper balance of the two hormones can be critical in determining whether a plant will survive or not. This is especially true in cases such as for mountain pine beetle and the elm bark beetle which act as carriers of devastating fungal pathogens such as the notorious Dutch elm disease responsible for nearly destroying the entire North American population of American Elm (Sherif, Shukla, Murch, & Bernier, 2016). The plant must therefore make a conscious decision as to which is the greater threat and the wrong choice can have fatal consequences, leading to a selective pressure for smarter plants.
A plant which fits most easily into the human perception of intelligence and reaction is the mimosa plant (Mimosa pudica L.) which responds rapidly to touch by closing its leaves. This plant is able to sense touch and by using electrical signalling, in a similar manner as it is employed in human nerve cells, it is able to response instantaneously. Mimosa is an especially interesting model as in addition to this rapid response, which is used as a defense mechanism in nature, it is able to learn and remember what stimuli are dangerous, and therefore worth the energy to respond to, and which may be ignored. Mimosa was first studied hundreds of years ago by the famous botanist Jean-Baptiste Lamarck, a familiar name to anyone who has taken a biology course, and then in the early 1900’s by the celebrated Indian biophysicist J.C. Bose, a leader in the field of plant electrical signalling and communication. More recently, it has been shown that in response to shaking or dropping of the plant, it will initially respond as expected, but after a certain number of drops the plant realizes that there is no danger associated and then ignores the stimulus, thereby saving energy. Most interestingly is that these plants not only learn in the moment, but when these plants were tested for their response even a month later, they had a memory of the non-threatening status of this stimuli and did not respond (Gagliano, Renton, Depczynski, & Mancuso, 2014; Shepherd, 2005).
Plants – manipulated or the manipulators?
Another interesting demonstration of plant intelligence is their ability to differentiate between friend and foe, and to communicate with them accordingly. This is seen in plants interactions with both other plants and with vertebrates and invertebrates such as birds, butterflies and honeybees as well as herbivores of both varieties. Essential oils are one very multicultural language used by plants to talk to, eavesdrop on and listen to all of these groups. These essential oils are made up of hundreds of compounds and the specific composition of an oil can relay very specific messages. A plant can simultaneously attract a pollinator to their flower by producing compounds, such as linalool, a bee pheromone or sex chemical, while announcing how unpleasant they are to eat, to a herbivore such as a mite or aphid using defensive compounds such as the small volatile aroma chemical, caryophyllene. This essentially allows the plant to communicate with insects or even birds or bats in their own language while at the same time coupling this chemical language to many other forms of communication such as the ultra violet markings seen on petals or choice of colour for fruit to attract just the right animal to transport their precious genetic material, thus ensuring their survival for generations to come. To make this communication even more complex, many of these compounds are extremely energy expensive to manufacture, with the colour indigo being one of the most costly to produce, and yet, plants choose to spend their resources on creating these compounds, and for very specific reasons. After all, if plants weren’t deriving some benefit from these processes, they would have long ago lost the battle for fitness, and natural selection would have removed them from the genetic pool.
The Real Mother Nature: do plants show kinship and altruistic behaviour?
Perhaps of the the most human, and thus in the eyes of humans, most definite demonstrations of intelligence is altruistic behaviour or kin recognition. It may surprise many in fact to know, that is behaviour is demonstrated in plants, unsurprisingly the old adage “no good deed goes unpunished” also seems to apply in plants with non-kin being able to eavesdrop in on these conversations. As discussed above, the essential oils of plants make up an incredibly complex language and in the case of many members of the Lamiaceae or mint family, in which this phenomenon was first observed, that language can be more specific to other individuals with a more similar genetic makeup. In these studies a sagebrush (Artemisia tridentata Nutt.) was injured in a manner similar to what would occur during herbivore attack and it was observed that the surrounding plants incurred less herbivore damage, suggesting that they somehow were able to sense the injured plant, and in turn raise their own defenses (Karban & Shiojiri, 2009; Karban et al., 2014). Follow up studies determined that it was the volatiles produced from the injured plant which signalled the surrounding plants and found that plants which showed identical genetic makeup responded more strongly to these volatile cues than non-relatives, thereby allowing the injured plant to give its own DNA a greater chance of surviving on, the most basic driver for any parent-child relationship. Though this response may be strongest among relatives, even other species, and in regard to this sagebrush example, wild tobacco (Nicotiana attenuata Steud.), are able to eavesdrop in on this non-verbal message (Karban, 2001). Another example of the ability of plants to differentiate between relatives, or more broadly their species and other species can be observed easily in any home garden. Take the example of seed germination, if a single pot is planted with all the same variety of seed, genetically similar individuals, the plants will moderate the spread of their roots and growth rates, to roughly allocate even resources for each seedling. If you were to plant a mix of seeds from different species, including your original species, in the exact same pot, the growth dynamics change rapidly. Instead of the community minded approach of giving each individual an equal shot at the available resources, namely space, light, water and nutrients (such as potassium and nitrogen), the seedlings will start to compete fiercely with each plant trying to gain the greatest space in the soil and largest overall biomass, and in some cases deliberately poisoning the other seedlings with toxic chemicals such as cinnamic acid (in a process called allelopathy).
If I only had a brain… or do they?
You may now be wondering how exactly is it possible for a plant to possess all these many faculties without some kind of central information processing centre, a brain! To address this concern, one must return to a consideration of the plant body plan, and at the most basic level, what differentiates plants from animals. It all boils down to motility, while animals chose to get up and run, walk or fly to gain the resources essential to life, namely food and water, plants took a sessile approach to the matter. Without specific adaptations for this lifestyle though, plants would have become the proverbial sitting ducks of the world, a snack for everyone, and again would have found their genes lost from the gene pool. Imagine the inconvenience if a plant were to a body similar to a human with a single centralized location for digestion (stomach), information processing (brain), and nutrient transport (heart). All that would be necessary would be for a herbivore to have a snack and the plant would be unable to recover, leading to death. Instead plants have adopted a body plan which was so eloquently described by the Greek philosopher Democritus as “humans with their heads in the ground”. Though we have learned much since then, the basic principle remains the same. Plants have an inverted and diffuse body plan as compared to humans, with the unifying principle being redundancy. In fact, instead of thinking of a plant of a single individual, it has been suggested that it is easier to think of a plant as a colony or a swarm, where there are many individual parts of the whole, none particularly significant on their own, but as a whole possessing incredible abilities. Instead of a single brain, plants contain many thousands or millions of information processing hubs which have been proposed to be located at the tip of roots, in a region called the transition zone. This zone is characterized by slow growth, a unique cytoskeletal arrangement and active vesicle transport closely resembling the synapses seen in the human nervous system with the primary neurotransmitter of these synapses being the universal plant growth regulator auxin, though plants have also been found to synthesize many of the human neurotransmitters including melatonin, serotonin, dopamine and adrenaline (Erland, Murch, Reiter, & Saxena, 2015; Kulma & Szopa, 2007). This zone is ideally located for its role as the neural center of the plant being located between the fast dividing root tip meristem, where new cells are produced by mitosis and the fast elongation in which these new cells rapidly elongate and finally mature. Additionally, the transition zone is the terminal receptor of the phloem, the nutrient trafficking vessels which transport nutrients and growth regulators (including auxin!) from the very tip of the plant, the apical meristem, and the leaves (Baluška, Mancuso, Volkman, & Barlow, 2009; Verbelen, Cnodder, Le, Vissenberg, & Baluška, 2014). This makes the transition zone a competent receptor of messages from aerial portions of the plant and at the very tip of the roots which are exploring their underground environment. The plant body plant is therefore defined as the anterior region being the roots, where information processing and nutrient acquisition occur and the posterior region comprising the aerial portions where reproduction and excretion (in particular gas exchange) occur, truly making them aliens with their head stuck in the ground.
How does one go about studying plant intelligence exactly?
Though plants demonstrate many of these processes one of the greatest difficulties in the advancement of the field of plant intelligence is the ability to study intelligence and its related behaviours in plants. The fundamental requirements for the study of plant intelligence are (a) an intelligent organism and (b) a challenging environment. While the former is present in all plant science experiments, the latter is often neglected, making the likelihood of observing an intelligent response unfavourable. This stems from the emphasis in the design of scientific experiments for controlled, consistent and favourable conditions. For plants this often means that all their needs are met, therefore, there is not need for a plant to demonstrate problem solving type behaviour, as they are able to recognize that they are in an environment in which all their needs are met, and no extraordinary measures are therefore required. A plant which is growing in the wild, in a challenging environment such as high salinity, extreme temperatures, drought or elevation, as is the case for many medicinal plants, is required to take many more intelligent steps to ensure their success and survival. Medicinal plants are by definition medicinal due to the unique properties, usually due to the unique compounds (phytochemicals), which they produce for the purpose of improving their own fitness. The unique nature of these compounds, and their important roles in adaptation and survival under stressful conditions, makes them excellent markers to observe for for the study of a plants choice of response. Medicinal plants, can therefore be utilized as a powerful tool for the study of plant intelligence.
Plants dominate Earth’s biosphere with more biomass being comprised of plants than any other living being, with estimates being as high as 99 %. This is not ecologically empty space, humans depend on plants for everything from medicines to shelter to food, and have taken great care to establish and spread anthropologically important plants from relatively small niches which they traditionally occupied, across every corner of the globe. We might consider ourselves the single greatest vector for the spread of plants such as corn, soy and wheat which are almost ubiquitously present. Considering this, only one question truly remains: who is really controlling who?