A major difficulty in studying any plant behaviour is that time scales differ from those in animals. Whereas human beings operate in seconds, plants usually operate in weeks and months. Even though bamboos can grow a centimetre an hour, without some sort of recording device it would be extremely difficult for any human to observe this phenomenon. Plant behaviour in the wild is usually unrecorded and, as a consequence, much uncommon behaviour must simply be missed. Time-lapse photography is at least a start, but how many plant physiologists with time-lapse facilities study and experiment on wild plants where real intelligent behaviour is to be expected? There is no doubt this is a serious omission in the scientific literature. There are so many crucial questions to pose. Why is it that one wild seedling survives and others do not, when apparently shed at the same time from the parent plant and in the same soil? There is so little information on the actual preliminary struggle for existence recorded in real time.
To the well-informed physiological reader not much of the information above will be especially new. However, the particular combination that I have presented here of intelligence, learning, memory and fitness should place some facets in a different light. Higher plants do represent about 99 % of the eukaryotic biomass of the planet. Their sessile life style is clearly successful and individuals must then possess a fine ability to adjust and optimally exploit the local environment. How well they map the local environment and the extent of computation (with good estimates of computational skill) clearly still requires significant investigation in real not artificial environments.
Undoubtedly, one of the problems that botanists have with using the words ‘plant intelligence’ are incorrect assumptions about animal intelligence, which is often equated with human intelligence and suppositions of complete freedom of choice (if they exist). Much animal behaviour is strongly heritable (for example, reproductive or early feeding behaviour is probably innate) and, indeed, has to be. So, in the same way, there are aspects of plant behaviour that are rarely phenotypically plastic. The structure of the flower is a good example, or the square-shaped stems of the Labiatae, among many. Apart from the fact that the major form of expression of animal intelligence is movement rather than growth and development, as defined here for plants, I find there is little to distinguish between the two groups of organisms once adjustments are made for the time differences noted above. As regards movement, the computer that beat Kasparov at chess (surely an excellent example of intelligence in action regardless of the human requirement to program) certainly required human intervention to move the pieces. We have already described the necessity for the right environment to elicit intelligent behaviour, and the Kasparov chess computer is again an excellent example. Good at chess, it wasn’t any good at assessing economics statistics until reprogrammed. Chess games were the right environment to elicit intelligent responses.
In fact, chess provides a further and important illustration of how ignoring individual behaviour and simply averaging behaviour can confuse understanding. Each chess game represents a unique and highly individual trajectory, recording intelligent behaviour between two properly matched opponents. Suppose instead that we now averaged 1000 chess games, much as physiologists average responses, and then looked for meaningful variations. The averaging process would reveal that pawns had a very high probability (and a narrow standard error) of being moved right at the beginning and the king being irreversibly confined (mated) at the end, although with greater variability. Knights and bishops would have a high probability of being moved early on, although the probability mean would be lower than that for pawns and the standard deviation broader. Castles (rooks) and queens would be later still and with much more spread in the standard deviation, and so on. In fact, averaging any one large set of chess games would look very similar to any other large averaged set, and we would conclude that the chess game on this basis was rote, started with a clock, of little interest and certainly nothing to do with intelligence. And, in an attempt to understand what was going on, we might experimentally knock out pieces only to find that, yes they were necessary and you lose if they go, just as we currently knock out cells, chemicals, genes or signal transduction molecules in an attempt to understand what is going on. Another crucial point is surely that very simple rules govern chess but the order in which events take place (i.e. the trajectory) can be unique to each game. This may represent a paradigm for signal transduction. We are so used to thinking of intelligence as a property of the human individual that we fail to recognize the necessity of applying that rule to plants as well.
Perhaps a more critical question is: does it matter whether intelligence is used to describe plant behaviour? If intelligent behaviour is an accurate description of what plants are capable of, then why not use the term? But, having used it, the next question is how it is accomplished in the absence of a brain. I have called this phenomenon ‘Mindless Mastery’ (Trewavas, 2002b) and can only suggest that intelligent behaviour is indeed an emergent property that results from cellular interactions, just as it is in the brains of animals. Whatever the mechanism, the end result usually comes from the distinctive behaviour of meristems. There must then be important conduits of proper information flow, as distinct from nutrients, from the rest of the plant into meristems.
Hopefully this article can indicate more clearly the kinds of investigations needed to fill in the gaps. Undoubtedly, we need very much more information on cellular and tissue communication and the distribution of receptors for all those signals that have been uncovered recently. We need many more studies on individual wild plant behaviour. Questions about tissue-to-tissue interactions need reformulating. How much information is conveyed between tissues, and what exactly is the sum total of its nature? Although the classic growth regulators are often assumed to carry out such communication, the uncertainty that still surrounds much of these notions is remarkable. Molecular studies can improve this situation, and some answers may arise from skilled use of inducible expression of tissue- and cell-specific critical synthetic enzymes. Other answers will arise from creative construction of particular environments in which plants can demonstrate their undoubted behavioural potential.
Although we understand much more about signal transduction processes in plants than we did 20 years ago, there is a long road yet to travel, to jump the gap between cell, tissue and whole organism. In this article I have travelled Robert Frost’s ‘less travelled road’. My hope is that, in future, this may become a more major highway.