Aspects of plant intelligence (ii)
Plant intelligence was earlier described as adaptively variable behavior during the lifetime of the individual plant (Trewavas 2003). This general definition for animals and plants (biological intelligence) is now justified from generic terms and emphasis on adaptive behavior. Plant intelligence can also be defined from dictionary definitions of intelligence. Artificial intelligence has been indicated as adaptive behavior. Prominent psychological opinion now indicates that human intelligence is adaptive: IQ does not measure human intelligence. The uniformity of intelligence definitions negates views that plant intelligence is controversial. It is suggested that the early stages of transduction through calcium are interpreted through complex protein structures attached to mobile lipid rafts. Cell signaling acting as a cognitive process is investigated and evidence supports a relationship. Plants are biologically purposeful; they express goal-directed behavior throughout their life cycle and act as biologically purposeful agents in the wilderness. The demise of the Modern Synthesis of Evolution is indicated and could be replaced by one that correctly emphasizes biological purpose. Two sensory mechanisms are described for gravitropism as an illustration of the fail-safe mechanisms needed for all forms of behavior because true wilderness is often environmentally uncertain. Definitions of learning and memory are suggested and five kinds of plant biological memories are described.
In this article, plant behavior refers to the total of responses by plants to a change in a signal or stimulus. Many behaviors involve changes in development eventually altering visible growth (so-called tropic responses) or other morphological features. This article concentrates on those behaviors that are adaptive; that is they improve the probability of survival of plants living in wilderness. 1 In Trewavas 2 these behaviors were classed as intelligent using the definition of biological intelligence as “Adaptively-variable behavior during the lifetime of the individual”. Trewavas 2 has been well-cited (currently 784, Google scholar) and it has generated considerable discussion in articles and books covering plant intelligence. Despite this degree of attention and debate much remains unsaid. Some regard intelligence as obvious while for other it remains apparently controversial.
This definition of plant intelligence, first suggested by Stenhouse 3 in reference to animal evolutionary behavior, is later justified for plants that live in natural, wild circumstances. Intelligence describes the wide ability of plants to manage the complex, uncertain, and often threatening challenges of the natural world in which plants struggle to survive and reproduce. To a very much lesser extent, it can accommodate the agricultural and other human-manipulated environments whose environmental complexity is substantially reduced. Adaptive behaviors, or behavioral traits, are behaviors that improve the probability of survival. 1 Adapt, or even acclimate, simply imply adjustment and do not replace the meaning and active implication of the word adaptive. Although adaptive capabilities can be investigated from laboratory research, such artifactual environments do not easily mimic the wilderness conditions in which biological intelligence contributes to differential survival. In my experience, the evolutionary context of “adaptive” is often not appreciated.
Some consider that the term intelligence for plants is subjective 4 , 5 based on the supposition that IQ subjectively measures human intelligence. Years earlier, Robert Sternberg, the most prominent psychologist and prolific supporter of IQ as human intelligence, had concluded that IQ did not measure human intelligence at all. 6 Sternberg 7 now concludes that real human intelligence is adaptive behavior and identifies the skills required to manage survival in real-world contexts. IQ simply measures scholastic aptitude 8 and is a psychological, not a biological, term. It has been described as a cultural artifact. 9 IQ, via its associated tests, was originally designed to help identify children who needed special educational help. There is also an argument over whether IQs are related to individual human social advancement or other human benefit. 10 IQ can only be used for one species: mankind. It cannot be used for the eight million or more species on earth.
When a zebra runs away from a lion, I regard that as intelligent behavior because it is adaptive. When I read that an ameba can immediately distinguish a Euglena cyst from a grain of sand of the same size and will devour the former while immediately rejecting the latter. 11 (p. 18), I see that as intelligent too. And that is important because plants evolved from an amebic ancestor. Darwin's (1891, p. 95–96) observations on tendrils actively exploring post holes to act as a support also describe intelligence. When one hole is found, the tendril assesses the size (diameter?) of the hole by attempted insertion. If this is too small, it searches for an alternative until one of suitable size and depth is finally found. 12 (p. 88). These examples of biological intelligence are each in their own, but different way adaptive; they improve survival probability.
The world we construct is the perceived world of an animal. The limitations of this perception for understanding plants are described elsewhere. 12 (p. 14–16). I cannot avoid the fact that, being an animal, I have to use a language constructed by other members of my species. That may be a serious perceptual constraint in trying to understand plants. Many zoologists are intrigued by what they regard as the complexity of animal life. Using the criteria of complexity and comparing angiosperms with mammals, a definite conclusion could not be reached as to plants being simple and animals complicated. 12 (p. 65–73). The angiosperm cell is likely as complicated as a mammalian cell or even more so. Understanding of either is still poor.
The difference between plant and animal behavior was clarified by Arber. 13 Most plant behavior is really development. Cell proliferation and subsequent differentiation commence in an embryogenic meristem. Cell maturation occurs in distinct and elongating stem and root tissues. From a human perspective, this process is inevitably slow. But the equivalent in animal development is usually slower. The zygote, enclosed in a protected environment of the egg or uterus, commences cell identification and tissue growth. It takes nearly a month for a young chicken to hatch or nine months for birth in mankind. Development continues after birth, increasing cell number in specified tissues as growth sets in. I consider the need for protection in early animal development to be the need for certainty of limb number. Movement is as crucial for animals as light is for plants. If limb number were highly variable, coordinated movement would be impossible and food and mate acquisition impossible too. It is only after birth that movement commences. Movement of animals is the recognizable but familiar characteristic that is coordinated by a nervous system that operates at similar speeds. Together with musculature, this determines the relative constancy of speed of animal movement.
There is no doubt in my mind that it is failure to visibly see general plant movement that leads to misleading designations of plants as simple and unintelligent. The behavior of plants is developmental, while animal behavior is only limited by the speed of action potentials and muscles. Although both are called behavior, strictly speaking they are not comparable. Time-lapse photography of plant behaviors belies human assessments of plants as still life. 12 (p. 13).
Animal complexity, if true, has its own hazards; more things to go wrong. The poor medical history of our species is strong support for this view. But the blame surely lies on an unbalanced evolutionary history; it's been rushed. Angiosperms appeared over 100 million years ago and have had plenty of time to sort out problems via evolutionary selection. The evolutionary history of homo sapiens is, at best, one twentieth of that and that is not long enough for significant selection to take its full toll. During that short period of evolution, the size of the brain has tripled along with a much heavier cranium and a poorly developed, S-shaped spine to support it when walking. It is an anatomical dysfunction known to cause very frequent medical problems. As for human intelligence which our species, Homo sapiens, places above all other organisms, past and present human history belies that assumption too. Wise we are not. Russell 14 considers that Homo faber (the craftsman) is a better designation of mankind. Our technology is superb. As a species, we are good at making things and taking others apart to see how they work. The natural human bent is mechanistic and reductionist. The zoological perception that animals are more complex, the greater the fascination in uncovering how it works. That probably explains why most biologists research animals; excepting obvious medical value. Reductionism indicates the failure to think in systems terms.
One common view, that can lead to botanical rejection, was to imply that plants were green animals. This was certainly the reaction to and the reason for rejection of plants as intelligent organisms. 15 The thinking that led to the intelligent plant in Trewavas 2 was fueled directly from experimental observations. Aequorin-transformed plants detected [Ca2+]I transients lasting some 20 seconds. The lag period in [Ca2+]I to a signal such as touch or brief wind stimulation was either a tenth of a second or less. How could something so fast lead in due course to something so slow as plant behavior? Eight different environmental signals generated transient kinetics in [Ca2+]I unique for each signal and it was clear that this was learning about the environment. 16 , 17 More significant were the observations that slight but selective inhibition of the [Ca2+]I transient to three different environmental signals blocked the induced transcription of genes normally associated with the specific environmental signal. 18-20 Changing gene expression can be slow and may account in part for the relative slowness of much plant behavior. But the phenomenon of priming results from altered gene expression and is now recognized as a prominent plant memory. 21
Bhalia and Iyengar 22 had described the emergent properties of the animal signal transduction network built around [Ca2+]I. This network is largely congruent to that known in plants. These authors concluded that signal transduction enables cells to learn about their environment and reported that an emergent property of this system was to construct a memory. This was referenced as an unusual form of intelligence, 17 because learning and memory are the essential bases of all forms of intelligence. On that basis, intelligent behavior via signal transduction networks was applicable to plants too.
By 1991, cell signaling through [Ca2+]I was already well-established in animal cells including nerve cells (e.g. 23-25 ). Nagata et al. 26 described 20 homologous genes involving calcium signaling between Arabidopsis and Homo sapiens. Many other homologous genes such as MAP kinases, protein kinases, phospholipase C, specific Ca2+channel proteins and others have now been detected in plants. One omission is an apparent absence of the GTP-binding protein, Ras, but there are other small GTP-binding proteins that may replace its function. The use of cyclic nucleotides in animal cells had been described by the middle 1950s and is now well-established as a signal transducer in plants too. 27 Nucleotide cyclases commonly act as specific developmental and metabolic receptors in both animals and plants, including single-cell plants e.g. Chlamydomonas. 28 The molecules to be sensed, however, do differ substantially between plants and animals. The expectation is retention of an enzymatic locus but modification of the remaining protein sequence to construct the specific sensor array, which has been found to be the case Gehring and Turek. 29
The divide between animal and plant eucaryotes is considered to have occurred at an amebic stage. Two billion years ago, an amebic ancestor engulfed a blue-green alga that with time evolved into the chloroplast via an intermediary symbiotic state. 30 , 31 That amebic ancestor clearly used [Ca2+]I as do present-day amoebae. 32 , 33 Paulinella is an ameba containing a captured cyanobacterial chromatophore acquired about 100 million years ago and a clear indicator of the mechanism of the critical first step in plant evolution. 34
Amoebae can associatively learn and that includes memory. 35 Such capabilities must have passed into the putative plant ancestor because they are still present in plants. The first indication of a short-lived, cold-induced memory was described. 18 Evidence for plant memories is now well established and described later. In this particular transduction and cellular context, describing plants as green animals is justified.
The definition of intelligence used by Trewavas 2 was constructed by Stenhouse 3 for a zoological audience. There were objections raised to its use because plants are not animals. 15 Objectors, however, failed to recognize the generic nature of the terminology used; adaptive, probability of survival, lifetime and individual refer to all living organisms and the “Individual” is characterized by Darwinian selection.
Life has a driving force built in; a fundamental property that underpins survival to enable reproduction. 36 The drive to survive was what enabled the evolution of life in the first place. It differs in intensity between individuals because of individuality, the molecular and genetic noise that results in individual variation. 37 , 38 Two examples exemplify the power of this drive to survive. Living bacteria can be found thousands of feet down in rocks 39 ; tardigrades resist freezing temperatures and the vacuum of space 40 amongst others. No life can exist without this fundamental capability.
Investigation dates the origin of life to about four billion years ago, not long after the earth itself was formed. Present evidence is based on identification of potential fossils in rock sections, 3.8 billion years old, accompanied by isotope discrimination between C13 and C12. 41 Stromatolites are clearly present by 3.5 billion years. Lepot 42 has illustrated some potential and unusual fossil structures of very early life. Kanaparthi et al. 43 suggest these look similar to lysed L-type bacteria. Life may have evolved without a wall and thus in low salinity environments.
Dill and Agozzino 44 identify the driving forces that underpinned life's origin. “We discuss four major prebiotic ‘discoveries’: persistent sampling of chemical reaction space; sequence-encodable foldable catalysts; assembly of functional pathways; and encapsulation and heritability. We describe how a ‘proteins first’ world gives plausible mechanisms”. The drive to survive and reproduce is basic to all life. Without that drive, there is no continuation of life.
Up to the present day, substantive environmental shifts have occurred resulting from continental drift, volcanic activity to variable extents, and damage by impacting extra-planetary debris. Douglass 45 illustrates a temperature history of Earth indicating that it has varied by at least 30 °C between epochs and has seen six cooling periods with five of them in the last two billion years including snowball earth. The origin of plants is placed at around 1.8–2 billion years ago. 31 Despite these severe environmental challenges, life continues because the earliest forms were built around mechanisms that confront and counteract the threats that abound. Evolutionary processes favor traits and behaviors that enhance individual survival and contribute to the potential maintenance of the species. Such behavior is also evident in our own species; the need for safety, food (energy), shelter, and reproduction often leads to a search for purpose and social connection that have direct biological origins. Adaptive behaviors (traits) increase the probability of survival of the individual during evolutionary challenge 1 but do not guarantee it.
Intelligence is “behavior that is adaptively variable during the lifetime of the individual” and I indicated it for adaptive behaviors in plants. 2 Survival and adaptive are generic terms. They apply to all present-day living organisms (plants, bacteria, protozoa, animals) that experience challenges to individual survival in wild circumstances and use adaptive behavior to increase the probability of survival. Biologists need to reject the one-species, human, veneer placed on intelligence and instead assess intelligence biologically. Life itself is intelligent and survived only because it evolved adaptive mechanisms. Earth is a planet dominated by plants; that is a good measure of evolutionary success and intelligent capability.
Stenhouse's book was published in 1974. The animal literature on behavior in 1974 tended to center around instinctual behavior, an heritable, apparently rigid behavioral pattern, sometimes assumed encoded in the genes and claimed to be a genetic blueprint. But instinct was still regarded as adaptive within the normal circumstances of the organism in question. Even 46 , (p. 237) saw the fallacy of these claims about the rigidity of instinctual behavior. The behavior of protozoa was commonly thought to be rigidly defined. But as Jennings 46 states “These ‘definable’ reaction forms are usually within themselves variable within wide limits.” Internal conditions and environmental changes are of the greatest importance in determining behavior. More recently, Lehrman's 47 withering criticism of instinct as proposed by Lorenz and Tinbergen emphasized instead the role of learning and development in these behaviors. Blumberg 48 provides an excellent critique of instinct concluding that they are not satisfactorily described as inborn, preprogrammed, hardwired or genetically determined; they are learnt during development. In Homo sapiens the only “instinctual responses” are the eye blink and the knee jerk which result from a reflex arc. Thus, Stenhouse arrived at behavior that was variable and adaptive, leading to improved survival during evolution that formed the books title.
The equivalent “instinct” in vascular plants might be the developmental cycle; seed to flower to seed. That seems naturally invariable in gymnosperms and angiosperms. A further equivalent “instinct” in plants might be the response to gravity. Virtually all plants are gravi-sensitive. Ma and Hasenstein 49 demonstrated that acquisition of seedling gravi-competency was determined by the position of the seed with respect to the gravity vector. If the embryo root pointed vertically upwards, only 25% of seed roots were able, in due course, to assume a downward growth direction. The most divergent form of behavior from supposed instinct is of course non-rigid, non-fixed; that is, variable behavior and the category that has most meaning for plants.
The Collins English dictionary (5th edition 50 ) states that intelligence is the ability to perceive and understand the “meaning” of that perception. Plants perceive enormous amounts of environmental information because they do respond positively to them. A list of environmental parameters that are sensed has been tabulated under ten different categories. 12 (p. 70). Perception of that information leads to physiological and phenotypic changes, many of which are clearly adaptive and can improve the probability of survival.
Kull 51 has provided a valuable article on the concept of biological “meaning.” He identifies the commonest biological use equates “meaning” to functional or purposeful correspondence. Since purpose is considered later, it is meaning as biological function correspondence that is considered here.
Using inbred lines of Polygonum cespitosum, Sonia Sultan 52 provided photographic examples of seedlings grown firstly, in dry (droughted) soil; secondly, in effective shade. The phenotypic changes were compared to controls experiencing optimal conditions for growth (These two photographs can also be found in Gilroy and Trewavas). 53
In drought conditions, the Polygonum root system was massively increased. The lack of water has been perceived and the meaning of that perception has led to massive root proliferation. A prime function of the root is to provide the plant with water. This is therefore an adaptive response and thus intelligent by the previous definition and that of the dictionary. The shoot is also massively reduced with probably increased cuticular thickness covering the few leaves. Premature flowering may provide seed that could, via transgenerational inheritance, be better adapted to the water-poor environmental conditions. Or they could remain dormant and only germinate when conditions improve.
There are correlative changes which result from the massive sequestration of carbohydrate for root proliferation. The lack of water is perceived first by the root meristems or early elongating root region. 54 Continuation of drought conditions leads to massive reduction of leaf synthesis with a thicker cuticle. These adaptive responses reflect species occupation of areas with uncertain or highly variable rainfall and involve eventual adaptive responses by the whole organism.
The second treatment was to place Polygonum plants in effective shade, thus severely limiting available light energy for photosynthesis. A primary function of leaves is to photosynthesize and provide the plant with carbohydrate resources. The reduced light intensity was perceived by the leaves (and possibly the stem) and transmitted to the shoot meristem. The meaning of that perception has been understood by the synthesis of leaves with greatly increased leaf area, thus compensating, in part, for the light-poor environment. Usually, such leaves are thinner with a reduction in the number of mesophyll layers. This intelligent adaptive response is to gather as much light as is possible in this light-poor environment. Again, these are adaptive responses.
The shade avoidance syndrome is an alternative but intelligent response to perceived shade that leads to an elongation of internodes with reduced thickness. The change in elongation rate might enable the individual plant to reach more satisfactory light regimes and eventually achieve greater seed number via greater flower exposure. There are simple relationships between gathered and stored resources and the number of seeds that can be provisioned.
In the two examples described, lack of water or light, the adaptive changes reflect attempts to overcome the environmental obstacles that hinder survival of the individual and, in turn, the species. Plants, by perceiving the resource imbalance and understanding the meaning of that perception by proliferation of roots or thinning of leaves, fulfill the dictionary definition of intelligence.