Smart plants: Memory and communication without brains

Abstract

The immobility of plants is consistent with their principal function: collecting light to provide photosynthetic substrate for the biological system. Their immobility does impose limitations on some basic requirements, such as the need for pollination, for seed dispersal, and for protection against herbivores. Meeting these 3 needs will logically necessitate some ability for plant communication – at least a capability for beneficial adaptive behavior. Three types of plant behavior provide evidence of memory and communication abilities: a capability for memory, a capability for measuring time, and extensive evidence of chemical signaling systems. These may provide benefits for genetic outcrossing, seed dispersal and protection – beneficial adaptive behaviors. The chemical signaling system constitutes a wireless communication network that draws mobile animals into assisting plant functions that require mobility. Plants share their chemical signaling systems most frequently with insects and birds. These beneficial adaptable behaviors may be interpreted as some type of consciousness.

Keywords:

• plant communication
• memory
• behavior
• chemical signaling
• seed germination

To begin this discussion on memory and communication abilities in plants, some definition of nomenclature is necessary. The use of the term intelligence is ordinarily restricted to human communication capabilities involving the brain – an example being measurements such as in IQ testing. For plants, a more relevant definition may be a capability for ‘adaptively variable behavior’, a term that has been proposed by David Stenhouse¹ and subsequently used by Anthony Trewavas.^2,3 It allows for learning by plants even in the absence of an organized brain. In essence, learning in plants can be considered to involve using information from the environment in order to make changes that can increase their fitness. Such changes would constitute ‘adaptive beneficial behavior.’^2-4

Considering the principal ecological function of plants to be the production of substrate for the community of organisms, their immobility is consistent with that primary role. However, immobility necessarily imposes some limitations. To meet these limitations, plants show evidence of being able to exercise adaptively beneficial behavior in several ways. Three impressive evidences of such behavior in plants are their ability for remembering, for time measurement, and for communication by chemical signals.

Plants Remembering

Evidence of remembering in plants is most evident in their movements. For example, the familiar ability of sunflower flowers to move in a manner that follows the sun is an obvious response to a diurnal light signal. Their flowers are directed to the easterly direction in the morning and they follow the sun to the west in the evening. During the subsequent night period, the flowers return to face the east.⁵ These return movements in the dark indicate that the flowers not only track the sun, but they anticipate the return of light, even when the light signal has not yet been restored. The plants remember the coming of morning.

Kalanchoe flowers also show diurnal cycling – being oriented upward during the day and downward during the night. If the plants are transferred to continuous darkness, the flowers continue the diurnal movements for several cycles.⁶ That plants continue cycling without a light signal indicates that the plants remember the daily light signal even after the signal has been discontinued. They remember the cycling of sunlight.

A similar situation is seen in the diurnal movements of leaves in many plants. For example, the leaves of Albizzia show diurnal changes in leaf position during the day and night. Again, the positional cycling repeats itself, and if one transfers the plant into darkness the cycling of leaf position continues for several day intervals.⁷ The cycling continues without the light signal, again indicating that the plants remember the cycling of light.

Seeds, too, can provide examples of remembering. For instance, in experiments with Polypogon monospeliensis (a native Israeli plant), seed dormancy is determined by the day length: short-days induce dormancy and long-days induce germination. Gutterman⁸ found that the photoperiod given to the parent plant determines the germinability of the subsequently matured seeds. Application of short-days (9–11 h/day) to the maternal plant induced dormancy in the subsequently produced seeds, and that dormancy of seeds could be shown to persist for 10 subsequent months. Gutterman and Gendler⁹ demonstrated that seeds of Mesembryanthemum nodiflorum in dry storage show a cycling between dormant and non-dormant states in line with annual seasons. They showed that the cycling of dormancy continued for more than 30 y in storage – a longer-term memory.⁹ These various adaptations to photoperiods constitute adaptive beneficial behavior.

Plants as Timekeepers

In addition to plants remembering, they have a well-known ability to measure time. For example, the seeds of Begonia remain dormant unless they experience long days. Darkness of more than 12 h (during a 24 h cycle) will induce dormancy, and the seeds will not germinate. Night lengths of 8 hours or less will completely break germination.¹⁰ Thus a 4-hour difference in night length completely regulates dormancy. The fact that these seeds can discriminate between night lengths differing by 4 hours, indicate an innate ability for time keeping, which constitutes adaptable behavior.

Knowing that the long night is an effective regulator of seed dormancy, experimental night interruption for Begonia seeds has provided evidence of a more precise time measurement. Under a 7-h-per-day light period (that is, a dark period of 17 h per day), the seeds remain dormant, but if a 30 min light interruption is applied at various times during the night, dormancy is relieved. A 30 min light experience in the middle of the night results in almost 50% germination. Interruption treatment at earlier or later times of the night results in lesser germination.¹⁰ This experiment illustrates that the seeds can discriminate between light interruptions applied at different times of night, with the middle-of-the-night being most effective, and other times of interruption being less effective. Therefore these seeds can discern not only the length of the night, but also they can respond selectively to light interruption at different hours of the night. In other words, the seeds can tell the time of night.

Another type of timing control of plants is the seasonal timing of plant flowering and death. An ordinary example of seasonal timing is the flowering and then the death of entire fields of wheat that occurs in July. Even in midsummer, the season of seemingly optimal growth, the thousands of wheat plants in a field all die in synchrony. This developmental change is linked to some internal calendar signal which causes fruiting and dying in the early summer – a seasonal timing. Adaptable behavior preempts longevity.

Some plants are able to count years. Annual plants flower in the first year, biennial species typically grow for 2 years, the first year being one of vegetative growth, and the second provoking flowering and subsequent death.¹¹ Other species keep growing for 3 or more years before blooming and then dying. The Century plant (Agave deserti) blooms and dies after about 50 y.¹² There is a rather famous claim that bamboo plants die in synchrony worldwide. Synchronous flowering and death is specific for this species, A. deserti. Other Agave species or variants flower and die after various times, ranging from 3 to 120 y. Only some species or races die en masse. Janzen¹³ points out that there is no evidence of any environmental cue responsible for the onset of bamboo flowering/dying, and he concludes that there must be some “internal calendar” – a perennial memory, distinctive to certain bamboo species.

A less visible example of timing is monocarpy in trees. As an example, the palm Corypha elata grows vegetatively for perhaps 40 y, and then flowers, fruits and dies.¹¹ Again, the tree apparently responds to some ‘internal calendar’ for tracking years or even decades of time: again an adaptable behavior.

Related to the issue of time-keeping is the capability for unusual long-term memory of suppressed growth. Pea plants show optimal growth under conditions of alternating diurnal day/night temperatures. When grown at a constant temperature, the growth is suppressed resulting in a dwarfing type of growth. We have no real understanding of the mechanism of dwarfing, but in peas the seeds from the resulting dwarfed plants produce progeny that retain the dwarfing form even when grown under the shifting diurnal temperatures. The dwarfing effect is inherited for 3 subsequent generations of peas.¹⁴ This quantitative alteration of growth is remembered and expressed for several subsequent generations. An analogous feature for remembering has been noted for Arabidopsis plants, which respond to radiation stress for successive generations – remembering across generations.¹⁵

This brief synopsis illustrates instances of plants having a memory, being capable of time-keeping over a range of hours, days or even decades of time. A type of dwarfing stress can even be remembered over generations.

Examples of the timing of the sequences that lead to an ending of the life-cycle occur in annual, biennial or perennial species, and even in trees. We utilize these life-cycle characteristics routinely in horticultural and agronomic programs, taking routine advantage of the plants’ beneficial adaptations to calendar-level timing.

Chemical Communications

The pervasive range of chemical emanations and communication has been described by Eisner and Meinwald¹⁶ who conclude that ‘all organisms engender chemical signals, and all, in their respective ways, respond to the chemical emissions of others. The result is a vast communicative interplay, fundamental to the fabric of life.’¹⁶ This interplay of chemical emissions is a major basis for beneficial adaptive behaviors between diverse organisms. In the last 2 decades, such interplay of chemical emissions has been increasingly understood as a communication base for plants, and similarly a dramatic range of communications between plants, insects and birds has been defined.^17-20

The emissions of volatile chemicals by organisms in general have led some scientists to write about plants “talking” to each-other, to insect herbivores and even to predators of herbivores. Utilizing changes in the landscape of chemical patterns can give rise to beneficial adaptations. This communication system has given rise to a proposal for the term, “plant neurobiology.”^21,22 As the awareness of nearby organisms is not dependent on nerves, the term is troublesome.

We humans are used to considering emissions of light and sound as the primary components of information about biological interactions occurring around us. The chemical emissions of Eisner and Meinwald¹⁶ provide an alternative basis for defining interactions of organisms in the chemical landscape. These landscape changes are impressively detectable by local chemistry. In a chemical landscape, there are potentials for communicative options (adaptive beneficial behavior), to achieve genetic outcrossing, to achieve seed dispersal, and to provide some levels of communication in the ecological community.

Exploiting animals for genetic outcrossing

Among plants, the most obvious example of chemical communication is the attraction of insects and birds which facilitate in floral pollination. In addition to the dazzling array of bright colors of flowers at the light level, there are also chemical emissions – the aromas of flowers. Contributions to the chemical landscape around flowers are commonly achieved by the emission of volatiles, acting as attractants for pollinators, and often with the promise of foods for the pollinators. At the chemical level these commonly involve emissions of phenols, glycoproteins, terpenoids and volatile fatty acids. Pleasing chemical attractants (e.g., the floral aroma of violets, iris, or vanilla), provide communicative linkages from plants to pollinator insects and birds.

In some cases floral aromas involve scents that are imitative (e.g., the odor of sexual attractants, odor of dung or carrion). Others serve as attractant enhancers through the production of heat (e.g., heat emissions of Arums such as skunk cabbage).^23,24 Among the most famous of the imitative type of attractant are the sexual stimulants that attract male eoglossine bees to visit some orchid flowers (e.g., Ophrys, Stanhopea, Gongora). The odor of these flowers contains volatiles such as methyl-cinnamate and cineole,²⁵ that may be sexual stimulants of bees themselves, or alternatively that may be converted into sexual stimulants by the male bees.

The effectiveness of floral volatiles from members of the Araceae is greatly enhanced by heat generation. This involves a cyanide-resistant type of respiration (alternative respiration) which can heat the flower by 4 to as much as 14°C²⁴ – enough to melt the snow around emergent skunk cabbage plants in winter, and at the same time enhance the effectiveness of the floral scent in attracting insects.

Nectar production by flowers is most common. It may be considered to be a component of the chemical information system, as it is the principal reward component for the pollinators. Nectar is usually composed of solutions of sugars – usually glucose, fructose and sucrose making up between 20 and 75% of the nectar solution. Proteins and amino acids or lipids are sometimes present.²³

It is surprising to find that the nectar may include repellant substances (e.g., nicotines) that serve as repellents to pollinators.²⁶ These substances serve to limit the amount of nectar consumed by pollinators, shortening the duration of pollinator visits, thus encouraging the pollinators to visit more individual flowers rather than staying too long at a single flower.^26,27

The flowering plants offer aromas and nectars that serve as attractants for insects and birds, providing chemical information, transmitted from the flowers to the pollinators, and achieving a beneficial adaptation.

Exploiting animals for seed dispersal

Among the benefits that plants offer to the animal kingdom are offerings of fruits – wonderful packages containing seeds, either embedded in the fruits (e.g., melons) or attached to the outside of fruits (e.g., strawberries). The strategy on the plants’ part is to provide edible fruits containing either large seeds which the birds or animal will spit out or drop, or else small seeds that animals can ingest, thus providing seed dispersal with the feces as the animals defecate at remote sites.

Novel intermediates occur in plants like violets, the seeds of which appeal to ants because of a small, attached lipid body, the elaiosome. With an appetite for the lipids, ants will carry the seeds away and store them, thus providing for seed dispersal.¹¹ As an alternative, the plant may produce seeds as a bur that becomes embedded in fur (or in clothing), and thus is dispersed – again to a distant place.

So, several options serve as beneficial adaptations to entice mobile animals that provide transportation services to the immobile plant either in response to chemical attractants such as aromas, or as edibles.

Chemical talking

Volatile emissions from plants can provide other services. They are often enhanced as a consequence of rupture of the plant tissue by herbivores. Tissue rupture commonly results in the release of volatile chemicals, as for example the synthesis of lachrymators by onion cells upon cutting. When plants are attacked by chewing herbivorous insects, the ruptured tissues experience major increases in the emission of volatile chemical signals.²⁸ An example is the production of ethylene resulting from herbivore action. The emissions of ethylene or other volatile chemicals can inhibit attacking insects.^29-31 The emissions can have inhibitory effect on the herbivore insects, and they can induce neighboring plants to also produce the emissions, making them less appealing to the herbivores.¹⁷ The emission from damaged plants can inform other plants downwind that herbivores are attacking.¹⁹ In addition, these same volatiles can inform predators that feed upon the herbivores.^18,32 The effectiveness of the attracting predators can be impressive. In one report the attraction of predator insects resulted in a 90% reduction in the number of attacking herbivores remaining on the leaf.¹⁹ In addition to ethylene production, 2 other compounds with strong plant regulatory effects have been detected in this communicative system: methyl salicylate and jasmonic acid.^20,33,34 Thus volatiles can provide a basis for “talking” among plants, and between plants and insects.

It is not surprising that the transfer of information by volatile chemical signals can involve genetic signals. Studying spider mite attacks on the leaves of Lima beans, Arimura et al.³⁵ found that attacking mites (Tetranychus urtice) caused an activation of 5 separate genes in the wounded leaves, resulting in the synthesis and release of defensive terpenoids. Artificially wounding the leaves did not cause the terpenoid effect.

As a parallel to the communication via chemical signals among the aerial parts of plants, there is at least one finding of chemical messaging that involves plant roots. Exposure of Arabidopsis roots to the pathogenic bacterium, Pseudomonas syringii, stimulates the formation of L-malic acid by the roots, resulting in the introduction of malate into the soil medium.³⁶ The malate in turn serves to recruit a beneficial bacterium, Bacillus subtilis, which serves as a protectant for the roots against the disease organism.³⁶ In this case, the plant responds to contact with a disease organism, releases a specific organic acid into the soil medium, which then recruits protection in the form of a beneficial bacterium. This remarkable communication between 3 organisms constitutes yet another specific benefit to the plant.

These various examples of communication between plants and their neighbors by means of chemical signaling provide beneficial functions in plant development and ecology. Such chemical signaling systems may be widespread among insect, fungi, and bacteria. The use of chemical defenses by insects are illustrative of ‘the vast communicative interplay’ of chemical ecology.³⁷ Thus plants are not alone in utilizing chemical messaging in the absence of a brain structure. A wireless communication system among organisms without structural brains may be very widespread.

Outlook

The term intelligence ordinarily implies the presence of a brain. In plants, with no identifiable brain structure, the term must relate to inferring a capability for beneficial adaptive behavior, whether or not there is a brain structure involved.

Literature of plant physiology has long included evidence of plant behavior that suggests benefits for adaptability. Examples include the evidences for memory in plants, and evidence that plants can keep time, or can be aware of seasons, and cycling of development. But perhaps the most extensive evidences of beneficial adaptive behavior by plants relate to changes in the chemical landscape – most frequently involving volatile chemicals that can yield information between organisms (e.g., information of attacks by herbivores) or alternatively that can provide mobile services to plants (e.g., promoting pollination and plant distribution).

In considering the ability for plants to communicate without a detectable structural sensor, analogy is seen in the communication systems between consortia of microorganisms.³⁸ In those cases, beneficial chemical communications are accomplished which involve capabilities to adjust to changes in environment modulated by an exchange of chemical signals. For example consortia of various bacteria (e.g., E. coli, Pseudomonas) are able to communicate with each-other, either by exchanging substrates, or more relevant to this discussion, by exchanging signaling substances (often complex carbohydrates and phenolics). In other words, communication between species of microorganisms in consortia seems to permit the performance of beneficial adaptive behavior.

The evidence for plants participating in wireless communication networks between one-another as well as with insects, provide examples of apparent ‘learning’ and a capability for chemical communication/interactions. Likewise there are precedents of chemical communication systems between microorganisms – even simpler organisms without any apparent structural basis.

Collectively they provide evidence of a wide array of organisms being able to communicate without any identifiable structural or neurological basis. Thus plants are not alone in utilizing intelligent actions via chemically based wireless. Plants share the benefits of wireless communication with most of the biological life systems, commonly the basis for adaptively beneficial behavior.

The omission of a structural equivalent of brain for intelligence is shared with a great diversity of organisms, including some invertebrates, fungi, bacterial and even protozoans. The existence of intelligent behavior may occur widely through biological systems, and is certainly not exclusively a feature of organisms that have defined brains.

Abram (1997) suggests that the world is made up of multiple intelligences.³⁹ The variable beneficial capabilities of plants as well as a wealth of less complex organisms, supports the position that multiple intelligences are indeed widespread in the biological world, and reaffirm the position of Eisner and Meinwald¹⁶ that ‘all organisms respond to the chemical emissions of others.’

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.