Plants are !ӣ$%%!^$ӣ [fill in the missing word]*

Plant Behaviour & Intelligence. Anthony Trewavas. Oxford University Press, 2014

Man is arguably happiest when the ‘natural’ order of all things is maintained and where his own dominion over the natural world – which is religiously endorsed in the Christian tradition in the Holy Bible (although apparently only over animals…) – is unchallenged. And no more so than when he believes himself to be the most intelligent being on the planet. Which is why it’s taken some time for him to acknowledge – if not fully accept – that other animals are also intelligent – e.g. chimpanzees and dolphins (although Man is still top dog – of course!). However, what (s)he – we! – seems really averse to is the notion that non-animal organisms might also be intelligent, particularly plants.

In this regard, battle lines were clearly drawn earlier this millennium when a piece penned by Brenner et al. (2006), advancing the notion of plant intelligence as the discipline of plant neurobiology, was attacked by a multi-authored collective of noteworthy names in plant biology (Alpi et al., 2007). The concept of plant neurobiology was not a literal transplantation of animal neurobiology to the plant domain; there are no actual brains in plants (despite Charles Darwin use of that term – e.g. Baluška et al., 2009) or nerves (but Chandra Bose has advanced the view that plant’s vascular strands might operate in that sense – e.g. Stahlberg, 2006), and despite the fact that the physiology behind the closing of the Venus’ fly-trap is akin to nervous transmission (e.g. Volkov et al., 2009).

However, Brenner et al. (2006) was provocative, and not only generated debate but also spawned a new organisation – the Society for Neurobiology in 2005 – with a ‘manifesto’ and its own academic journal – Plant Signaling & Behavior. But, why was there such opposition to the notion of intelligent plants? Surely, it wasn’t just down to the language – metaphorical though it was (Trewavas, 2007) – used by its proponents *. So, why should there be such resistance to that idea? Well, opposition and ‘slings and arrows’ there be, so the best way of dealing with that is to “take arms against a sea of troubles, and by opposing end them”. And Trewavas’ Plant behaviour & intelligence (the book’s emphasis…) [hereafter referred to as PBI] surely does just that, and counters that blinkered view of plants and their ‘abilities’.

I’m not a plant neurobiologist but approach my assessment of PBI as a botanist who wants to know more of the “complexity and controversy of plant behaviour” (from PBI’s back cover text). So, wide-eyed and open-minded, what does PBI deliver?

Technical stuff

PBI’s 26 chapters are spread over 291 (+ xii) pages, so each is relatively short, and intended to be ‘read’ as stand-alone items. After some scene-setting subjects like The origins of photosynthesis; Why did plants become multicellular?; and Are angiosperms more complex than animals?, subsequent chapters deal with particular facets of plant behaviour and intelligence, e.g. The varieties of plant behaviour; Self-organization and behaviour in root systems; Behavioural characteristics of seeds; Games plants play; Brains and nerve cells are not necessary for intelligent behaviour; Intelligent genomes, and Intelligence and consciousness.

Reference citations are fully integrated within the chapter and listed at the end of the relevant chapter (so the chapter is truly stand-alone). And the references are reasonably up-to-date; there’s a high percentage of post-2001 dated ones. However, there are few post-2010. This surprised me; surely there would be many more recent ones to back-up the claims of the new way of thinking about plants? But, reflecting further, I realised that notions of plant intelligence and behaviour aren’t that new (merely newly resurrected); this is not a 21^st century ‘eureka moment’ of profound insight, but rather a rediscovery of work done often many years previously which had largely been overlooked or dismissed at the time. And PBI’s apparent 6 years’ gestation period would presumably have given the author opportunity for updating the text with more recent studies – if they existed.

The book concludes with 10.25 pp. of 3-columned Index. Whilst it may be unsurprising that there is no entry for Arabidopsis here (Trewavas is not a fan of this ‘weed’), it is surprising that neurobiology doesn’t feature either (although references thereto are cited on pp. 157 and 265). Unusually for a book that deals with quite technical topics, PBI has no glossary – you may have to ‘google’ unfamiliar terms, though for the most part they are explained where essential.

My assessment of PBI

Let’s get the ‘contentious’ stuff out of the way first. For Trewavas’ purposes, behaviour = what plants do (“the organism dealing with the perpetual problems thrown up by its environment, regardless of whether movement in response is obvious or not”, p. 74) (see also Trewavas, 2009); and intelligence = capacity for problem-solving (“intelligence is based on how efficient a species becomes at doing the things they need to survive”, p. 76) (see also Trewavas, 2003; 2005). I.e., no neurobiology, no provocative pronouncements, no misleading metaphors, just unambiguous, uncontroversial, straightforward, telling-it-as-it-is, statements of fact. And it’s also important to bear in mind that for Trewavas ‘plant’ is synonymous with an angiosperm, specifically an undomesticated dicot. In particular, Trewavas is quite keen on trees – as exemplified in his impressive listing of 35 points of similarity in structure, behaviour, reproduction and defence between a deciduous tree and self-organising insect colonies.

Using those definitions, and whilst acknowledging that plants are different from animals, PBI claims that plants are nonetheless intelligent and perfectly well-behaved organisms. An extraordinary claim? Probably. Is it justified? Well, they do say that extraordinary claims require extraordinary evidence, and that’s what PBI delivers. In a manner akin to the mass of evidence assembled by one Mr C Darwin in support of the concept of evolution via natural selection, Anthony Trewavas (FRS, FRSE, and Professor Emeritus at the University of Edinburgh, Scotland, UK) has accumulated an overwhelming (surely?) and dazzling array of observations and published research in support of the book’s subject matter. And in so doing he has constructed a powerful argument that plants do behave and are intelligent, and this should no longer be ignored, or dismissed as some inconvenient truth.

Along the way, PBI provides some uncomfortable reading and has some interesting thoughts on the value of averaged data (p. 144), provides a good assessment of limitations of controlled experiments to explore real examples of plant intelligence (pp. 244-245), and makes the point that memory of previous conditions (which has different periods of its retention, from seconds to months, to years…) can complicate and compromise assessment of plant response to conditions in the here-and-now (p. 274). In fact, taking all of this together, one could become completely experimentation-averse (which would never do – how would science advance then?)! But, recognising the bias we generate when using Arabidopsis – a pioneer, weed species whose intensive study has narrowed both our focus and our expectations/realisation of what plants can actually do (!) – as standard experimental material (p. 249), there is a need to establish that what works in Arabidopsis actually applies in a ‘proper’ plant, in the real world. Which should encourage more experimentation. However, Trewavas cautions against using domesticated plants for experimental purposes since the domestication process usually involves elimination of numerous behaviours (i.e. they aren’t proper plants in this respect). With PBI’s emphasis on undomesticated, truly ‘wild’, plants and how they behave in nature, it is refreshing to see the role of ecologists and field-based investigators favoured over more laboratory-based enquirers. It’s also welcome to see an emphasis on cells and whole organisms/ecology in PBI rather than this being yet another tome that extols purely the molecular side of life (although this aspect gets a good airing when calcium signalling is considered in chapter 25).

There is a saying that one shouldn’t judge others by one’s own standards. That can be extended in this instance to don’t judge plants by human standards (or by what our own senses can detect/react to). And it’s the refusal to comply with that principle that underlies much of our resistance to recognising plant behaviour and intelligence; we tend to use subjective human criteria of behaviour to judge other organisms, rather than recognising that plants behave, but in ways that are unfamiliar. This human view of behaviour is, well, anthropomorphic and altogether too simplistic: If things don’t move, they don’t behave (although, as Trewavas argues, plant changes with growth are akin to animal movement). For a supposedly emotionally-detached, objective activity like science, scientists are curiously and stubbornly subjective when faced with the thought that organisms other than animals can actually behave, intelligently.

As Trewavas recognises, the widespread commonplace negative view of plant intelligence/behaviour is to some extent reinforced by the simple and uncritical way in which textbooks and teaching deal with the subject matter (p. 249). As botanists we rightly object to ‘plant blindness’ [e.g. Allen, 2003]. But, surely, uncritical, knee-jerk denial of such notions as plant intelligence and behaviour is also an example of that phenomenon. All that Trewavas is doing is to ask us to re-examine well-known, established phenomena and to look with fresh eyes. And what’s wrong with that? Trewavas doesn’t force us to ask whether plants are more intelligent than animals, rather just to acknowledge that plants are intelligent and should be accorded that recognition. Whilst I don’t claim to follow every example used in the book I do appreciate the overall thrust of the argument, and am convinced enough of the importance of the message, that plants are intelligent.

So, have we missed this plant behaviour hitherto? Or just not recognised it? Or resolutely refused to interpret it correctly (after all, there are none so blind as those who will not see)? Maybe a bit of all of the above. And without intervention – e.g. books such as PBI – the situation if likely to get worse. One of PBI’s great strengths therefore is the many examples used to support the idea of plant intelligence and behaviour. I’m not able to vouch  for the veracity of all of them, and Trewavas’ interpretation needs to be vigorously challenged and assessed (that, after all, is only good and proper science) to the satisfaction of even his sternest critics. And, as Trewavas himself often concludes, the details of how the processes work are unknown. But this is not to admit defeat and say that one should give up. Rather, there is the challenge to future researchers to probe the system, using all the modern-day techniques we possess, discern the details, and establish the validity (or otherwise…) of the claims.

Comparisons?

In terms of the breadth of scope and weight of evidence brought to bear on its subject matter, PBI is probably unique, and therefore without compare. However, a likely companion is Karban’s Plant Sensing and Communication (which I’ve not yet read). Mancuso and Viola’s Brilliant Green: The surprising history of plant intelligence seems to be an interesting addition to PBI (but which I’ve also not yet read…), and Chamovitz (2012) is a useful book to set the scene for PBI’s more hard-hitting thesis and synthesis.

Overall view

Plant behaviour & Intelligence is designed to be challenging and more than a little provocative (and controversial even), but it deserves to be read by all who want to understand how fascinating and worthy of study plants are. And PBI makes you think. It doesn’t demand that you become fully paid-up members of the Plants are Intelligent Club, but does expect that you read, mull over and carefully consider the material assembled, and form your own view (though it’s clear what that view should be!). What more could one ask of a non-fiction book? Although PBI contains “merely subjects that interest the author” (p. ix), they are topics that should interest all those who wish to understand plants better. Biologists everywhere (but especially zoologists or zoo-minded botanists) should read – and heed – this book. Interestingly, the title page declares this to be the First Edition. Clearly, updated, subsequent editions are envisaged by the publisher. And why not, this is surely an area of study that – like its subject matter – will only grow!

Final words

“Plant intelligence is one of those categories described as aberrations, but when properly investigated will start to reveal how a complex non-neural organism derives intelligent behaviour from the systems structures within itself. The challenge is there. What is needed is the devotion of open-minded, imaginative individuals to take the challenge up” (Trewavas, p. 278).

References

Allen W (2003) Plant Blindness. BioScience 53: 926-926.

Alpi A, and 35 others … (2007). Plant neurobiology: No brain, no gain? Trends in Plant Science 12: 135–136.

Baluška F, Mancuso S, Volkmann D and Barlow PW (2009) The ‘root-brain’ hypothesis of Charles and Francis Darwin Revival after more than 125 years. Plant Signaling & Behavior 4: 1121-1127.

Brenner ED, Stahlberg R, Mancuso S, Vivanco JM, Baluška F and van Volkenburgh E (2006). Plant neurobiology: An integrated view of plant signaling. Trends in Plant Science 11: 413–419.

Chamovitz D (2012). What a plant knows: A field guide to the senses. New York, NY: Scientific American / Farrar, Staus & Giroux.

Stahlberg R (2006) Historical Overview on Plant Neurobiology. Plant Signaling & Behavior 1: 6-8.

Trewavas A (2003). Aspects of plant intelligence. Annals of Botany 92: 1–20.

Trewavas A (2005). Plant intelligence. Naturwissenschaften 92: 401–413.

Trewavas A (2007). Response to Alpi et al.: Plant neurobiology—all metaphors have value. Trends in Plant Science 12: 231–233.

Trewavas A (2009). What is plant behaviour? Plant, Cell & Environment 32: 606–616.

Volkov AG, Carrell H, and Markin VS (2009) Biologically Closed Electrical Circuits in Venus Flytrap. Plant Physiology 149: 1661–1667.

* INTELLIGENT

** One notes with a certain wry smile that the Society for Plant Neurobiology did change its name, to the Society of Plant Signaling and Behavior in 2009. Undeniably, intelligent behaviour by the plant neurobiologists.