Darwin's Most Wonderful Plants: A Tour of His Botanical Legacy 9780226675701

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Darwin’s Most Wonderful Plants

Darwin’s Most Wonderful Plants DARWIN’S BOTANY A Tour 0f His BotanicalTODAY Legacy

KEN THOMPSON

th e u ni versity of chicago p r e ss

The University of Chicago Press, Chicago 60637 © 2018 by Ken Thompson The moral right of the author has been asserted. All rights reserved. No part of this book may be used or reproduced in any manner whatsoever without written permission, except in the case of brief quotations in critical articles and reviews. For more information, contact the University of Chicago Press, 1427 E. 60th St., Chicago, IL 60637. Published 2019 Printed in the United States of America 28 27 26 25 24 23 22 21 20 19   1 2 3 4 5 isbn-13: 978-0-226-67567-1 (cloth) isbn-13: 978-0-226-67570-1 (e-book) doi: https://doi.org/10.7208/chicago/9780226675701.001.0001 First published in Great Britain by Profile Books Ltd., 2018. library of congress cataloging-in-publication data Names: Thompson, Ken, 1954– author. Title: Darwin’s most wonderful plants : a tour of his botanical legacy / Ken Thompson. Description: Chicago : The University of Chicago Press, 2019. | Includes bibliographical references and index. Identifiers: lccn 2019009778 | isbn 9780226675671 (cloth : alk. paper) | isbn 9780226675701 (e-book) Subjects: lcsh: Darwin, Charles, 1809–1882. | Plants. Classification: lcc qh31.d2 t44 2019 | ddc 576.8/2092—dc23 lc record available at https://lccn.loc.gov/2019009778 This paper meets the requirements of ansi/niso z39.48-1992 (Permanence of Paper).

CONTENTS Introduction The Secrets of Plants

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7

Chapter 1 Room at the Top ............................................................ 23 On the movements and habits of climbing plants (1865)

Chapter 2 Slow Learners

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69

The power of movement in plants (1880)

Chapter 3 The Biter Bit

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103

Insectivorous plants (1875)

Chapter 4 Sex and the Single Plant

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156

On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing (1862) The effects of cross and self-fertilisation in the vegetable kingdom (1876) The different forms of flowers on plants of the same species (1877)

Chapter 5 The Mysteries of the Cabbage Patch ......... 214 The variation of animals and plants under domestication (1868)

Afterword ........................................................................................................... Sources ............................................................................................................... Photo Credits ............................................................................................... Thanks .............................................................................................................. Index ..................................................................................................................

227 230 241 244 245

INTRODUCTION

The Secrets of Plants

I

f you were writing a book about almost any aspect of the natural world, you could do a lot worse than start with Charles Darwin. And not only because he was the author of The Origin of Species, a book that – ultimately – explains everything. Darwin’s consuming interest in evolution fed, and in turn was fed by, an almost obsessional curiosity about natural history. Much of this extraordinarily broad interest in the natural world, it’s true, was motivated by a search for evidence for evolution by natural selection.To take one small example, a problem that bothered Darwin (and was used as a stick to beat him by his critics) was the very wide distribution of some kinds of animals and plants. How to explain the presence of a species in two or more widely separated locations (and sometimes 7

INTRODUCTION

nowhere in between), other than that was where a Creator had chosen to put them? Part of the answer lies in plate tectonics, but that discovery lay over a century in the future (one problem with being ahead of your time is having to wait for others to catch up). Another part of the answer is dispersal: the underappreciated ability of species to travel very large distances, often in unexpected ways.To see if seeds might be dispersed by ocean currents, Darwin spent over a year testing the ability of seeds of many species to survive immersion in sea water. He also suspected that seeds might disperse in mud stuck to the feet of wading birds, many of which were known to migrate over huge distances. But are there seeds in mud? Nothing for it but to find out: I have tried several little experiments, but will here give only the most striking case: I took in February three table-spoonfuls of mud from three different points, beneath water, on the edge of a little pond; this mud when dry weighed only 6¾ ounces; I kept it covered up in my study for six months, pulling up and counting each plant as it grew; the plants were of many kinds, and were altogether 537 in number; and yet the viscid mud was all contained in a breakfast cup! Considering these facts, I think it would be an inexplicable circumstance if water-birds did not transport the seeds of fresh-water plants to vast distances, and if consequently the range of these plants was not very great. 8

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That’s it – Darwin had no more to say on the subject, but those few words had fired the starting gun for the study of soil seed banks, now a thriving sub-discipline of plant biology and ecology. Sometimes Darwin seemed to stumble on a whole area of biology almost by accident. For example: I had originally intended to have described only a single abnormal Cirripede [barnacle] from the shores of South America, and was led, for the sake of comparison, to examine the internal parts of as many genera as I could procure.

Describing one barnacle, one imagines, would hardly have taken him too long, but that entailed a comparison with other barnacles, one thing led to another and the eventual result, taking eight years’ work, was a two-volume monograph on this enormous class of crustaceans, running to well over 1,000 pages. Already, we can begin to see some characteristic features of the Darwinian approach: an astonishing capacity for hard work (Thomas Edison’s dictum that ‘Genius is one per cent inspiration, ninety-nine per cent perspiration’ could easily have described Darwin), and an unwillingness to take anything on trust. He was unimpressed by mere scientific reputation, but once persuaded that someone knew what they were talking about, he was happy to correspond with anyone from gardeners to pigeon fanciers. But if Darwin wanted to 9

INTRODUCTION

know anything, his usual response was ‘let’s find out’, and woe betide any idea that failed to stand up to experimental scrutiny. Thus his attitude to homeopathy, as fashionable among the scientifically illiterate then as it is now, was blunt: [It is] a subject which makes me more wrath, even than does clairvoyance. Clairvoyance so transcends belief, that one’s ordinary faculties are put out of the question, but in homœopathy common sense and common observation come into play, and both these must go to the dogs, if the infinitesimal doses have any effect whatever. How true is a remark I saw the other day by Quetelet, in respect to evidence of curative processes, viz. that no one knows in disease what is the simple result of nothing being done, as a standard with which to compare homœopathy, and all other such things.

Another consistent feature of Darwin’s work was that, irrespective of his original motivation, he tended to fall in love with whatever he happened to be working on at the time, until it became an overwhelming passion. The barnacles were no exception; how else to explain the eight years he spent working on them? After a period of ill health, he wrote in March 1849 that he was looking forward to getting back to work on his ‘beloved barnacles’. Mind you, Darwin was as capable as the rest of us of biting off more than he could chew. Towards the end of 1849, there’s a hint that barnacles 10

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are less fun than they were: ‘my daily two and a half hours at the barnacles is fully as much as I can do of anything which occupies the mind’, and by 1852 the love affair was well and truly over: ‘I am at work at the second volume of the Cirripedia, of which creatures I am wonderfully tired. I hate a barnacle as no man ever did before, not even a sailor in a slow-sailing ship.’ By 1855 his relief is palpable that ‘I have at last quite done with the everlasting barnacles’. Barnacles may have been one of Darwin’s early passions, but later that enthusiasm was transferred to other branches of natural history. Many of these later love affairs were botanical, initially at least because plants were convenient experimental material. As his son Francis put it after his father’s death, Darwin determined to learn about plants ‘as he used them in the building of his theory’, but later on ‘the tables were turned, and the theory served him as a powerful engine to break still further into the secrets of plants’. Not that Darwin ever pretended to be a botanist; he had no professional training in the subject, and was amused to receive accolades from ‘real’ botanists and botanical institutions. But Darwin’s love of the natural world knew no boundaries, and he was as capable of falling in love with a plant as he was with a barnacle or an earthworm. One of the great advantages of knowing little or nothing about a subject, of course, is that you can 11

INTRODUCTION

An illustration by George Sowerby from the second volume of Darwin’s barnacle book. Darwin himself was a poor artist and his own sketches that appear in his books are rudimentary.

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approach it with fresh eyes, and a mind free of (often erroneous) preconceived ideas. But ignorance can only take you so far, and it was his (and our) great good fortune that Darwin’s botany was guided throughout his life by Joseph Hooker, Director of Kew Gardens, a man who really did know his botany. Indeed, if you want a biography of Darwin, one that gives you a real feel for how he spent his time, his correspondence with Hooker would do as well as anything else. By the 1860s, with The Origin of Species (the first edition anyway) and the everlasting barnacles out of the way, Darwin was free to indulge a serial love affair with a range of different kinds of plants, an affair that would single-handedly revolutionise much of the science of botany. His letters reveal that in 1860 carnivorous plants were his passion, that he had been ‘infinitely amused by working at Drosera [sundew]’, ‘working like a madman at Drosera’, and that his ‘beloved barnacles’ had become his ‘beloved Drosera’. Unlike barnacles, however, carnivorous plants seem to have retained Darwin’s enthusiasm; even much later in 1874 his opinion of a day working on the carnivorous bladderwort was that ‘I have hardly ever enjoyed a day more in my life than I have this day’s work’. But even bladderworts paled beside the Venus fly-trap, which ‘from the rapidity and force of its movements, is one of the most wonderful in the world’. At other times, Darwin’s overwhelming passions were climbing plants, 13

INTRODUCTION

orchids and even the pollination of primroses, each of which, for a time, occupied him to the exclusion of everything else. Of course, any fool can be impressed by a Venus flytrap. Darwin’s genius was to see the wonder, and the significance, in the ordinary and mundane, in things that you and I wouldn’t look at twice. To take one example, the great theme of chapter three of The Origin of Species is the ‘struggle for existence’. In Darwin’s own words in The Origin: ‘Hence, as more individuals are produced than can possibly survive, there must in every case be a struggle for existence, either one individual with another of the same species, or with the individuals of distinct species, or with the physical conditions of life.’ This is the ‘selection’ in natural selection: only a minority – often a tiny minority – of plants and animals live long enough to leave any descendants. Thus the gleeful satisfaction with which Darwin received any evidence of the natural world’s propensity for the mass slaughter of young organisms. For example, in his own garden, as he reported in a letter to Hooker in 1857: Out of sixteen kinds of seed sown on my meadow, fifteen have germinated, but now they are perishing at such a rate that I doubt whether more than one will flower. Here we have choking which has taken place likewise on a great scale, with plants not seedlings, in a 14

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bit of my lawn allowed to grow up. On the other hand, in a bit of [bare] ground, 2 by 3 feet, I have daily marked each seedling weed as it has appeared during March, April and May, and 357 have come up, and of these 277 have already been killed, chiefly by slugs.

In short, trying to create a wildflower meadow by sowing seeds into established grass is a mug’s game, and most seedlings, if unprotected, are eaten by slugs. Neither of these observations will raise even one eyebrow among seasoned gardeners; and yet, to Darwin, they represented two key pieces in the developing puzzle that was evolution by natural selection. Nor did Darwin leave the puzzle there; to him, all this suggested another question, as we can see later in the same letter: ‘What a wondrous problem it is, what a play of forces, determining the kind and proportion of each plant in a square yard of turf! It is to my mind truly wonderful.’ For, as Darwin realised, if the fate of most seedlings is to be eaten by herbivores or annihilated by other plants, and the race goes to the biggest, toughest plants, how do we explain turf with thirty or more species in a square yard (for such turf does indeed exist)? That question has occupied entire scientific careers ever since, including part of my own, and still provokes violent disagreement. And finally to the biggest question of all. Darwin concluded his letter with ‘And yet we are pleased to 15

INTRODUCTION

wonder when some animal or plant becomes extinct’. In other words, for wild plants and animals, life is a precarious business, with death lurking round every corner. Thus it’s not at all surprising, indeed absolutely inevitable, that less well-adapted forms are constantly going to the wall and being replaced by those better adapted. In short, natural selection in a nutshell, and all from commonplace observations that many gardeners make every day. We’re never going to see plants through Darwin’s eyes, but in this book I hope to get as close as we can, and try to share at least some of the wonder and excitement that Darwin experienced, and to appreciate the originality and remarkably enduring value of his research. How to do this? Sometimes I think a simple account of what Darwin did, and of what he discovered, is sufficient. For example, although science has inevitably moved on in all the areas of biology that he studied, Darwin’s work on climbing plants was so far ahead of its time that it hardly needs updating. Even now, much of what we know about climbing plants goes right back to Darwin’s 1865 book, and if you were planning a PhD on climbing plants today, Darwin remains the foundation. He asked questions about how climbers know what to get hold of (and what not to) that we’re only beginning to answer. He also noted that almost all twiners twine in the same direction. But one of Darwin’s many virtues was not to lose any sleep over questions that were 16

THE SECRETS OF PLANTS

Darwin (right) at his home, Down House, with the geologist Charles Lyell and botanist Joseph Dalton Hooker, painted by Victor Eustaphieff.

not amenable to experimental investigation. Twining direction is probably one of those questions, and we still don’t know why most plants twine the same way. Where things have really moved on since Darwin’s time, the cause is often the advance of technology. For example, some recent research on the extremely clever nanoparticle composite glue used by ivy to stick to trees and walls used (among other things) a Phenomenex 17

INTRODUCTION

BioSep-SEC-S4000 silica gel filtration column, an Agilent 6000 ILM/AFM equipped with Nanosensors PPP-NCHR-20 silicon cantilevers with spring constants of 4–20 Nm-1, and a Malvern ZetaSizer Nano ZS (the latter, naturally enough, to measure the zeta potential of the ivy nanoparticles). All followed by a spot of scanning electron microscopy. You really do need this kind of kit to produce the necessary evidence, so it’s clear why Darwin’s investigations of plant glues – with his brand of country house, kitchen-sink experimentation – was never going to make much headway. Something else that has changed is that the modern world is a smaller and much more thoroughly explored place, so we now know about plants that simply hadn’t been discovered in Darwin’s time. Today, the two common Wisteria species grown by gardeners are so familiar and ubiquitous that it comes as a shock to realise that Darwin was acquainted with only one of them – and was thus unable to think of an example of twining climbers in the same genus that twine in opposite directions (as the wisterias do). Completely unknown in Darwin’s day was the chameleon vine, a tropical climber with the scarcely credible ability to mimic the plants it uses as a support. (And even with modern experimental equipment, no-one has the first idea how it does such a thing.)

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The same themes loom even larger when we look at carnivorous plants where, as usual, Darwin was far ahead of his time; before his work, it wasn’t even generally accepted that carnivorous plants were carnivorous. Because plant carnivory so completely up-ends the normal order of things, all carnivorous plants are intrinsically fascinating, but we are now familiar with several examples that were unknown to Darwin. One bizarre example is a tropical climber that’s only a parttime carnivore, and also climbs by means of leaves modified into grappling hooks. (More about this plant, Triphyophyllum peltatum, in Chapter Three.) It’s also interesting to take a look at plants that Darwin could have considered but,for whatever reason,chose not to. He almost completely ignored pitcher plants, for example, in both their temperate and tropical manifestations. In this book, I’ll look at some of the recent research on their use of chemical warfare and intricate partnerships with everything from ants to bats and tree shrews. The advance of technology has changed our understanding of carnivorous plants too. It’s fascinating to look over Darwin’s shoulder as he tried to work out how the underwater traps of bladderworts work. In the end he failed, but it was hardly his fault; bladderworts are the fastest carnivorous plants on the planet, and our present understanding of how they work (which is fair but still

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INTRODUCTION

hardly complete) has had to await the arrival of cameras capable of taking thousands of frames per second. Another technological advance is the entire science of genetics. Speculating about the evolution of carnivorous plants, Darwin got a lot right, but it’s easy to be fooled by appearances, especially when looking at plants that have adopted unusual lifestyles such as carnivory. You can’t blame Darwin for thinking that all carnivorous plants with sticky tentacles were related to each other, but our modern ability to peer directly at DNA reveals that they’re not. Elsewhere in this book I will explore similar themes in other aspects of Darwin’s work, where one constantly discovers subjects in which he was first in the field, and where his work often leads down surprising botanical byways. We’ll see what came of his famous prediction that an orchid flower with a 30-cm nectar-containing spur must be pollinated by a moth (then undiscovered) with a 30-cm tongue.We’ll see how Darwin worked out the significance of the unusual arrangement of the male and female parts of primrose flowers, when no-one else appreciated that this arrangement needed explaining. We will even see that, foreshadowing a debate that has really only developed in recent years, he was sure (and with good reason) that plants are intelligent. Along the way we’ll see how Darwin’s work transformed horticulture,

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and helped to inspire a scientific approach to gardening by the Royal Horticultural Society. Because Darwin’s work on evolution by natural selection was so brilliant, it’s easy to overlook all this work. Nothing, of course, can compete with his evolutionary achievements; even Darwin could only shake the world’s foundations once. But his botanical work is as impressive as everything else he did.You may

Two illustrations of sundew (Drosera rotundifolia) from Darwin’s book on insectivorous plants.

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INTRODUCTION

admire Darwin already, you may be familiar with The Origin of Species, but it’s unlikely that you know Darwin the botanist. I hope to change that, and in the end we will agree, I hope, that Darwin’s ‘most wonderful’ plants are just as amazing as he thought they were, and that even if he had never written The Origin of Species, Darwin would still rank as one of the greatest biologists who ever lived.

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CHAPTER

1

Room at the Top On the movements and habits of climbing plants (1865)

W

hy was Darwin interested in climbing plants? There’s the connection to natural selection, of course, and the gradual modification of leaves (and other structures) into climbing aids. Indeed as we will see, Darwin thought that when it came to the gradual transformation of a structure evolved for one purpose into one modified for something quite different, vines offered about the best example anyone could wish for. But to a large extent it was the barnacle story all over again; he got started and found he couldn’t stop. The initial spur, in 1858, was a short paper by American botanist Asa Gray on the tendrils of a plant in the 23

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marrow family. Darwin grew some seeds Gray sent him, and was immediately ‘fascinated and perplexed’ by the movements of the tendrils; they looked complex, but he suspected that some simple principles were at work. And that was it, he was hooked: ‘I procured various other kinds of climbing plants, and studied the whole subject.’ And when Darwin says ‘the whole subject’, he really meant ‘the whole subject’. Darwin had already been working for years on pollination of orchids, and his reaction to some of the mechanisms of pollen transfer in that great group of plants was that ‘I never saw anything so beautiful’. But he went on to conclude that ‘Some of the adaptations displayed by climbing plants are as beautiful as those by orchids for ensuring cross-fertilisation.’ And for Darwin, that beauty is the key; any product of natural selection, performing a vital function with economy and elegance, was a thing of beauty. I can only agree. Climbing plants are beautiful, and wonderful – and addictive too, as Darwin discovered.

 Twining plants Right at the start of The movements and habits of climbing plants, Darwin observes that climbing plants come in various sorts, and that twining is ‘the largest subdivision, and is apparently the primordial and simplest condition of the class’. He reasoned that if you wanted to turn a 24

CLIMBING PLANTS

non-climbing plant into a climber, the simplest way to do that would be to have it twine; all the other options require more radical modifications. He next observed that in the hop, a typical climber, the young shoot ‘may be seen to bend to one side and to travel slowly round towards all points of the compass, moving, like the hands of a watch, with the sun’. His reaction to this observation shows just what a careful scientist Darwin was. For of course, the question is: how does this movement occur? Contemporaries of Darwin tended to assume that the stem itself twisted. It’s easy to believe this because, as Darwin noted, ‘the axes of nearly all twining plants are really twisted’. But he also noted that they weren’t twisted enough; a stem may have undergone thirty or more revolutions, but show evidence of only two or three twists. Ergo, the twisting and the revolving of the shoot are not related. In fact the twists are the simple mechanical outcome of wrapping a stem around a support, but the revolutions are caused by a zone of growth moving around the stem, alternately pushing the growing tip over to one side. Thus the revolving movement is more accurately described, as Darwin put it, as a ‘continuous bowing movement directed successively to all points of the compass’. The purpose of this movement, of course, is to increase the chances of bumping into a support. But 25

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more than that, it holds the key to twining itself. As usual, some of Darwin’s contemporaries had the wrong idea, assuming that the stems of twining climbers must be sensitive to touch (in Darwin’s word, irritable), so that they actually bend towards any object they touch. But Darwin couldn’t persuade twining stems to respond to anything, and concluded that twining round a support was just a natural extension of the normal revolving movement. Or, as he put it: If a man swings a rope round his head, and the end hits a stick, it will coil round the stick according to the direction of the swinging movement; so it is with a twining plant, a line of growth travelling round the free part of the shoot causing it to bend towards the opposite side, and this replaces the momentum of the free end of the rope.

This worked so well that Darwin concluded that irritability was unnecessary, a sentiment he expressed in classic Darwinian style: I conclude that twining stems are not irritable; and indeed it is not probable that they should be so, as nature always economizes her means, and irritability would have been superfluous.

Which also explains something important to gardeners. If a twining stem really did hug a potential support, in the hope that it might eventually travel right round and 26

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come back to where it started, it might by such means manage to hang on to even a very thick support. But, Darwin found, this was not so: I placed some long revolving shoots of a Wistaria [sic] close to a post of between 5 and 6 inches [13-15 cm] in diameter, but, though aided by me in many ways, they could not wind round it. This apparently was due to the flexure of the shoot, whilst winding round an object so gently curved as this post, not being sufficient to hold the shoot to its place when the growing surface crept round to the opposite surface of the shoot; so that it was withdrawn at each revolution from its support.

In other words, the normal revolving movement is enough to cause a stem to wrap itself round a support, provided that support is relatively narrow; but beyond a certain diameter, although the moving zone of growth starts out by pushing the stem towards the support, it soon pushes it away again, and no twining is achieved. So Darwin had shown, to his own satisfaction, that twiners were unable to attach to thick supports, something that many gardeners will confirm from their own experience. But he was uneasily aware that he had been able to experiment only on temperate climbers, and that the tropics were full of climbers, some of them enormous. Could they do things that temperate climbers couldn’t? 27

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To find out, Darwin did what he usually did when he had a botanical problem; in November 1864 he wrote to Hooker at Kew: Answer this only if by chance you can so surely that I may give it on your authority. — Can any spirally twining plant (not having tendrils) twine round a tree or post one foot or upwards in diameter? Our temperate climbers cannot, from a peculiarity in their movements, twine round a post even six inches in diameter. I suspect some of the Tropical Twiners can manage a much greater diameter. — Are there thick columns in the Houses at Kew?

Hooker replied with a mixture of his own observations and those reported to him by others, but Darwin was suspicious of third-hand data, and Hooker’s observations contained an important caveat: ‘We have columns of 6 in. in our houses & have climbers on some, but these have been helped, — whether necessarily or no I will not say.’ That ‘help’ is crucial; with enough coercion, twining climbers can be made to perform all kinds of tricks. I’ve seen both our commonly cultivated species of wisteria wound round thick columns at West Dean Gardens in Sussex, but they had plainly been strongly ‘encouraged’ to do so; one clear sign of this was that both were (by chance) growing in the wrong direction (see next section). So although Darwin reported Hooker’s 28

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observations in Climbing Plants, he was inclined to trust his own experience, which told him that neither wisteria, nor honeysuckle, nor several other species could be persuaded of their own volition to climb up anything more than about 11-12 cm in diameter. The inability of twiners to grasp wide supports, even in the tropics, has been confirmed by more recent research. In one study in Ecuador, lianas were found growing on trees up to a metre in diameter, but the largest trees supported only root climbers, which are not limited by host diameter. It was also obvious that twiners on wide hosts were relatively thick themselves, indicating that they had started out on thinner hosts and that the two had grown together. If we look only at thin twiners (less than 1 cm diameter), which had presumably colonised their hosts relatively recently, 90 per cent grew on hosts of less than 8 cm diameter. Twiners may also get into the crowns of big trees by using smaller trees, or even other climbers, as ‘ladders’.

 Twining left and right So twining stems revolve and, once they hit a support, this revolving leads naturally to twining in whichever direction they had previously been revolving. But which direction is that? Darwin carefully observed numerous twiners, classifying them as twining ‘with the sun’ or ‘against the sun’. There’s nothing wrong with those 29

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labels, but they do mean different things in the northern and southern hemispheres, so it’s probably a better idea to have a description of twining direction that works anywhere. A commonly used terminology is clockwise or anticlockwise, but that’s even worse. Because now, instead of just knowing which hemisphere you’re in, you need to know whether you’re on the floor looking up a climbing stem, or up a ladder looking down. Does the earth rotate clockwise or anticlockwise? It depends

Left and right-handed twiners: left, black bryony (Tamus communis); right, runner bean (Phaseolus coccineus).

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which pole you’re looking at. A better way to describe twining direction is as left-handed or right-handed. In other words, does the twining stem cross the support from lower left to upper right (right-handed), or from lower right to upper left (left-handed).This always gives the same result, irrespective of where you’re standing, or which hemisphere you’re in. There are two popular notions about which way plants twine. One, probably the more widespread, is that plants track the apparent daily east-west movement of the sun across the sky. Indeed only the other day, I read a newspaper description of a hop grower carefully helping the young hop stems to twine so that they track the sun (as if they needed any help, or that you could possibly persuade them to do anything else). The other idea is that it’s all determined by the Coriolis effect, which is what makes your bathwater drain in different directions (allegedly) in the northern and southern hemispheres. The latter hypothesis predicts right-handed twining in the northern hemisphere and left-handed twining in the southern hemisphere. Predictions of the sun hypothesis are more complicated, but you would still expect the direction of twining to vary with hemisphere and latitude. In 2007, New Zealand ecologist Angela Moles published a paper showing that about 92 per cent of the world’s twining plants twine in a right-handed 31

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helix, and this is true everywhere on the planet, so both hypotheses are wrong, and hops are in the small lefthanded minority. But Darwin’s observations, 140 years earlier, already strongly hinted at a preponderance of right-handed climbers; of the 40 species he studied, 27 were right-handed and 13 left-handed (if the appropriate statistical test had been invented at the time, this difference would have proved to be significant: i.e. the proportions of left and right-handed twiners was not random). In fact Darwin seems to suggest that this was old news even then: ‘A greater number of twiners revolve in a course opposed to that of the sun, or to the hands of a watch, than in the reversed course, and, consequently, the majority, as is well known, ascend their supports from left to right’ (my italics). Curiously, Darwin noted ‘I have seen no instance of two species of the same genus twining in opposite directions, and such cases must be rare’. One of the species he describes is Wisteria sinensis, which he correctly notes is right-handed. The Chinese wisteria was introduced to Britain in 1816, and by 1835 was widely available, so it’s not surprising that Darwin knew it. Down House, Darwin’s home in Kent, is today home to a large Chinese wisteria, and the romantic in me would like to believe that it was planted by Darwin himself. Unfortunately, although old watercolours and black and white photographs show Down House covered by 32

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Wisteria sinensis – which, as Darwin noted, twines right – growing on the garden wall of Down House, his family home.

climbers, these are all long gone, and we don’t know what they were. A photograph from as recently as 1994 shows Down House completely devoid of climbers, so its present covering must all date from its acquisition in 1996 by English Heritage, and it may just be an accident that the wisteria is the ‘right’ one. It’s a pity that Darwin was writing just too soon to be aware of the Japanese wisteria, W. floribunda, which wasn’t introduced from Japan (via the Netherlands) 33

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until the 1870s, so he was unaware of its left-handed twining (which thus allows it to be separated from its Chinese cousin, even when completely leafless). Undoubtedly, however, Darwin was right that two species in the same genus twining in opposite directions must be rare; I don’t know of any apart from wisteria. Collectors of botanical trivia will be delighted to learn that any hybrid of Japanese wisteria inherits its twining direction from that parent.

 Right-handed nature The fact that different plants twine in different directions would be interesting even if it were (apparently) random, with half going one way and the other half the other way. But the overwhelming predominance of one direction leads to the obvious question: why? Since twining has clearly evolved independently on many occasions, with very different plants as the raw material, why do we nearly always end up with a right-handed spiral? Surprisingly, this doesn’t seem to be a question that bothered Darwin; he simply notes that most twiners are right-handed and leaves it at that. Or is it surprising? Darwin was intensely curious about almost everything, but he was also always on the lookout for adaptive reasons for why plants and animals had turned out the way they had. Maybe he reasoned 34

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that it was hard even to imagine an adaptive explanation for left or right-handedness, and even harder to imagine any way of investigating it. Left-handedness may be rare, but there’s no evidence that it’s done the plants that have it any harm; both the climbing honeysuckles in my garden seem happy enough, despite their sinister habits. And you can’t make a plant change its mind to see what happens – the result of any attempt to do so is a plant that refuses to climb at all. In fact, even today we don’t really know why most plants are right-handed, but nature often is; most people are right-handed, and more than 90 per cent of snail shells coil in right-handed helices. It may simply be that nature is often right-handed at some fundamental molecular level; the DNA molecule is a right-handed helix, although left-handed DNA is theoretically possible. The basic building materials of life are proteins, themselves constructed from a small palette of amino acids. Amino acids, like most organic molecules (e.g. sugars) can come in two forms, which share exactly the same formula but are mirror images of each other. The two forms are called L and D and, while it’s tempting to think of them as left and right-handed, they aren’t in any real sense. The interesting thing is that life uses only the L forms of amino acids (no-one really knows why), and when L-amino acids come together to 35

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form proteins, they form a right-handed helix, usually called an Ơ–helix. There are proteins with left-handed Ơ–helices, but they are very rare. It’s easy to assume that all this underlying handedness, or chirality, must somehow give rise to the commonlyobserved right-handed behaviour of animals and plants. Chinese researchers have tried to trace the twining behaviour of gourd tendrils back to the helical angle of cellulose fibrils at the subcellular level, but I confess that I find their argument hard to follow. For all I know, maybe it goes all the way back to gravitational waves and the Higgs boson or whatever, but if it does then so far no-one has proposed a plausible mechanism. What is abundantly clear, over 140 years later, is that Darwin was probably right to consider the whole question to be one that probably wasn’t worth investigating, especially not with the technology available at the time.

 Tendrils As much as Darwin was entertained by twiners, he found that plants that climb using tendrils were even more absorbing. In the first place, tendrils illustrate a crucial feature of natural selection, which is that when faced with some new need, animals and plants rarely evolve some completely new structure or behaviour. Almost always, some existing structure is modified to meet the new requirement. Indeed, the world would 36

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be a very different place if living organisms had been designed from scratch, and the endless ways in which old structures are modified for new purposes, often in the most surprising and tortuous ways, is one of the most convincing pieces of evidence that none of them was designed at all. For example, the tiny bones that transfer sound vibrations to the eardrum in mammals started out as part of the reptilian jaw. The tendrils of climbing plants illustrate this principle perfectly. Many tendrils, perhaps the majority, are clearly modified leaves, for example those of the pea. Indeed in some climbers the tendrils are still leaves, but modified to have grasping stalks, as in all the climbing species of clematis. In other climbers, tendrils are equally obviously derived from flower stalks, or peduncles. The author of The Origin of Species was clearly delighted to discover that ‘If the genus Vitis [vines] had been unknown, the boldest believer in the modification of species would never have surmised that the same individual plant, at the same period of growth, would have yielded every possible gradation between ordinary flower-stalks for the support of flowers and fruit, and tendrils used exclusively for climbing. But the vine clearly gives us such a case; and it seems to me as striking and curious an instance of transition as can well be conceived.’ Nor is this the end of the power of modification illustrated by tendrils. Although grasping twigs and 37

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branches is obviously the primary function of tendrils, once plants have them, they can be adapted for quite different purposes. The tendrils of Virginia creeper, Ampelopsis hederacea (now Parthenocissus quinquefolia), observed Darwin, are not very keen on getting hold of a stick in the normal manner: When they meet with a flat surface of wood or a wall (and this is evidently what they are adapted for), they turn all their branches towards it, and, spreading them widely apart, bring their hooked tips laterally into contact with it. In effecting this, the several branches, after touching the surface, often rise up, place themselves in a new position, and again come down into contact with it. In the course of about two days after a tendril has arranged its branches so as to press on any surface, the curved tips swell, become bright red, and form on their under-sides the well-known little discs or cushions with which they adhere firmly.

Darwin was impressed by the remarkable tenacity of these adhesive tendrils: the tendril … rapidly increases in thickness and acquires great strength. During the following winter it ceases to live, but adheres firmly in a dead state both to its own stem and to the surface of attachment … The gain in strength and durability in a tendril after its attachment is something wonderful. There are tendrils now adhering to my house which are still strong, and 38

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have been exposed to the weather in a dead state for fourteen or fifteen years. One single lateral branchlet of a tendril, estimated to be at least ten years old, was still elastic and supported a weight of exactly two pounds.

 Tendrils in action Not only are tendrils one of the best examples of evolution in action, Darwin also found their behaviour fascinating. For, quite unlike the dull, insensitive stems of twiners, tendrils are exquisitely sensitive, responding to a light brush with a pencil, or to a loop of thread weighing only a few grams.The response could be quite sudden; in Passiflora gracilis (annual passion flower), for example: The movement after a touch is very rapid: I took hold of the lower part of several tendrils, and then touched their concave tips with a thin twig and watched them carefully through a lens; the tips evidently began to bend … in half a minute after a touch. One of the tendrils which thus became bent in 31 seconds, had been touched two hours previously and had coiled into a helix; so that in this interval it had straightened itself and had perfectly recovered its irritability.

In the real world, where plants are almost always in constant motion owing to wind, a tendril must often make contact with a support, but fail actually to grasp it properly. So, not surprisingly, disappointed tendrils are 39

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able to keep trying, over and over again. In the annual passion flower, for example, ‘To ascertain how often the same tendril would become curved when touched …

Flower-stalk of a vine, one branch with flower buds, the other modified into a tendril. From Darwin’s book on climbing plants.

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the extremity was gently rubbed four or five times with a thin stick, and this was done as often as it was observed to have become nearly straight again after having been in action; and in the course of 54 hours it answered to the stimulus 21 times, becoming each time hooked or spiral.’ If you wanted an image of what a dogged observer of nature Darwin was, you surely couldn’t do better than picture him constantly returning to watch a single passion flower tendril for 54 hours. Darwin also noted that although typical tendrils would grab hold of almost anything, they were also capable of remarkable powers of discrimination: I repeated the experiment made on the Echinocystis, and placed several plants of this Passiflora so close together, that their tendrils were repeatedly dragged over each other; but no curvature ensued. I likewise repeatedly flirted small drops of water from a brush on many tendrils, and syringed others so violently that the whole tendril was dashed about, but they never became curved.

Professor D. T. MacDougal of the University of Minnesota, working not very long after Darwin, around the turn of the century, found that tendrils fail to respond not only to rain, but also to ice. More recently, French botanist Antonin Tronchet, working at the Université de Besançon in the 1960s, found that tendrils of Passiflora coerulea (common passion flower) coil only around a steady support. 41

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In every case the adaptive value is fairly clear; a plant gains nothing from trying to grasp a passing raindrop or hailstone, it’s almost certainly a bad idea to try to grab an unstable support or one that whips about in the wind, and the botanical equivalent of trying to lift yourself up by your own bootstraps must also usually be a waste of time. In short, plants show every sign of intelligence, but what’s less clear is how they do it. Darwin guessed that it was the sheer brevity of a raindrop impact that led to a lack of response, but it’s not quite obvious how a plant manages to ignore ice but will still grab, say, a glass or plastic rod. Maybe temperature has something to do with it; other studies have shown that warmer tendrils generally work better than colder ones. The ability of tendrils to recognise – and ignore – tendrils from the same plant may seem surprising at first, but it probably shouldn’t. The ability to distinguish self from non-self is a universal feature of both plants and animals, central to the operation of the immune system and the ability of plants to reject ‘self ’ pollen and thus avoid self-fertilisation. These are genetically determined mechanisms that operate via proteins on cell surfaces; maybe tendrils work the same way … but then again, maybe not. For example, work in the last twenty years has shown that roots are very good at recognising roots from the same plant and thus altering their behaviour to avoid pointless competition for the same nutrients and 42

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water. But this is not based on the chemical recognition of a genetically identical individual; once cuttings from the same plant are separated, they become progressively more ‘foreign’ to each other and eventually treat each other as genetically alien plants. So self/non-self discrimination in roots seems to depend on physiological coordination among roots on the same plant, via a so far unknown mechanism. Are tendrils like that? Recently a Japanese team determined to find out, using the vine Cayratia japonica. Cayratia, a tendril climber in the vine (Vitaceae) family, has the useful ability to spread by underground rhizomes. This allowed the researchers to create variations on the self/non-self theme, ranging from tendrils on the same shoot at one extreme, to plants from completely different populations at the other. In between were tendrils from the same plant, but connected only below-ground, the same but with the below-ground connection severed, and plants from the same population (and thus presumably genetically distinct, but probably sharing a few genes). What did they find? Essentially, strong support for the idea that self/non-self discrimination depends mostly on physiological coordination, as in roots. Tendrils showed little reaction to tendrils to which they were connected below-ground, and even less to tendrils from the same shoot. But tendrils were far more likely 43

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Cayratia japonica – a species of herbaceous plant native to Australia and Asia, commonly known as ‘bushkiller’.

to react to tendrils from separate plants, irrespective of whether this was a genetically identical plant or one from a completely different population. But the reaction is far from black and white, and it’s interesting to find that tendrils showed a small response even to other tendrils on the same shoot, while at the opposite extreme, tendrils were more likely to grasp a bamboo cane than any other Cayratia tendril, however distantly related. 44

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There are two striking things about this research. One is that as much as the results support the physiological coordination hypothesis, this vine can still tell the difference between its own species and an inanimate or living but completely unrelated support, and much prefers the latter. We have no idea how it does this, but some chemical signal may be involved, and it may not even require contact. In much the same way, volatile chemicals from sagebrush (Artemisia tridentata) plants that have been attacked by herbivores induce resistance to herbivores in other nearby sagebrush plants, but genetically identical plants respond more than unrelated ones.The second is that this work is a lovely example of how, even in the twenty-first century, really interesting results can come from careful but essentially very lowtech experiments. Indeed, this whole study is one that it’s easy to imagine Darwin himself conducting. How does tendril coiling actually occur? Some of Darwin’s contemporaries thought it was all a result of growth, with the outer (convex) side of the coil growing faster than the inside. Darwin observed that ‘Sachs [Julius von Sachs, the German botanist regarded as the founder of modern plant physiology] attributes all the movements of tendrils to rapid growth on the side opposite to that which becomes concave.’ But, despite professing his humility on the subject, Darwin wasn’t so sure: ‘It is rash to differ from so great an authority, but 45

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I cannot believe that one at least of these movements – curvature from a touch – is thus caused.’ His reasons were various, but: One of my chief reasons for doubting whether the curvature from a touch is the result of growth, is the extraordinary rapidity of the movement. I have seen the extremity of a tendril of Passiflora gracilis, after being touched, distinctly bent in 25 seconds … It appears hardly credible that their outer surfaces could have actually grown in length, which implies a permanent modification of structure, in so short a time.

It’s worth noting that Darwin’s humility in the face of Sachs’ opinions may have been somewhat feigned, since they didn’t get on; Sachs basically thought Darwin was a hopeless amateur. In fact modern work has tended to support Darwin’s opinion that the initial, very rapid coiling is mainly a hydraulic-driven contraction on the inner (concave) side of the tendril, caused by loss of water from the cells on that side. The later response, measured in hours rather than minutes, is driven by growth of the outer (convex) side of the tendril. A related question is how tendrils detect the touching signal in the first place. In white bryony (Bryonia dioica), there appear to be special touch receptors, referred to variously as ‘tactile bleps’, tactile papillae or ponctuations tactiles. Tactile bleps are dome-shaped outgrowths of 46

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the peripheral cell wall of the outer (epidermal) cells of tendrils. Very similar structures have been described on the tendrils of the unrelated Chilean glory flower, Eccremocarpus scaber. How they actually work still remains something of a mystery, but as in excitable animals cells such as muscles and neurons, generation of an action potential seems to be involved. An action potential is an electrical signal caused by the rapid movement of positive ions from one side of a cell membrane to the other; in a neuron it’s the movement of this action potential down the axon that transmits a nervous signal. In animals the positive ion involved is potassium, but in plants it appears to be calcium.Transmission of the touch signal also seems to involve plasmodesmata, microscopic channels that allow transport and communication between plants’ cells, and possibly also fibres of actin, one of the proteins involved in muscle contraction.

 Coils and more coils But for tendrils, catching and coiling around a support is only half the story. As Darwin observed, once a tendril is firmly attached,‘a tendril … which has caught a support by its extremity … invariably becomes twisted in one part in one direction, and in another part in the opposite direction; the oppositely turned spires being separated by a short straight section.’ And: ‘Whether the spires turn once or more than once in 47

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opposite directions, there are as many turns in the one direction as in the other.’ He continues: We can now understand the meaning of the spires being invariably turned in opposite directions, in tendrils which from having caught some object are fixed at both ends. Let us suppose a caught tendril to make thirty spiral turns all in the same direction; the inevitable result would be that it would become twisted thirty times on its own axis.This twisting would not only require considerable force, but, as I know by trial, would burst the tendril before the thirty turns were completed. Such cases never really occur; for, as already stated, when a tendril has caught a support and is spirally contracted, there are always as many turns in one direction as the other; so that the twisting of the axis in one direction is exactly compensated by the twisting in the opposite direction.

Seeming to think that none of this was exactly obvious, Darwin was at pains to explain what was going on by analogy: Take a piece of string, and let it hang down with the lower end fixed to the floor; then wind the upper end (holding the string quite loosely) spirally round a perpendicular pencil, and this will twist the lower part of the string; and after it has been sufficiently twisted, it will be seen to curve itself into an open spire, with the curves running in an opposite direction to those round 48

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the pencil, and consequently with a straight piece of string between the opposed spires. In short, we have given to the string the regular spiral arrangement of a tendril caught at both ends.

Darwin then goes on to provide another analogy, involving ribbon-winding by haberdashers, but I’m sorry to say that it didn’t make any sense to me. What Darwin seems to have been trying to say, but somewhat struggling to find the right words for, is that once each end of a tendril is fixed, if the tendril is to coil any further, the formation of two oppositely handed helices, connected by a reversal, is a topological necessity. To Darwin, the adaptive significance of this spiral contraction was clear: A far more important service rendered by the spiral contraction of the tendrils is that they are thus made highly elastic. As before remarked under Ampelopsis [Virginia creeper], the strain is thus distributed equally between the several attached branches; and this renders the whole far stronger than it would otherwise be, as the branches cannot break separately. It is this elasticity which protects both branched and simple tendrils from being torn away from their supports during stormy weather.

In other words, the spirally contracted tendrils tension the whole plant, rather like adjusting the guy ropes on a tent or the rigging of a ship, so that all parts take their share 49

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A tendril of white bryony (Bryonia dioica), showing spiral contractions in reverse directions. From Darwin’s book on climbing plants.

of the strain. Not only that, but the spiral tendrils also act as springs, expanding and contracting as the plant is blown around by the wind. A remarkable illustration of the adaptive value of this spiral contraction, not lost on Darwin, was that despite having evolved independently in many quite unrelated plants, and often with very different origins, the great majority of (though not all) modern tendrils, once attached to a support, now complete their development by performing the same spiral contraction. The few species that do not show spiral contraction tend to have branched tendrils, and it may be that the extra grappling points are an alternative way to achieve secure attachment. 50

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It’s only relatively recently that we’ve begun to understand how spiral contraction works, but recent work on cucumber tendrils reveals that the key is special wood fibres called g-fibres. G-fibres are characteristic of reaction wood in trees, which is wood that forms in response to a specific stress rather than as part of normal growth. For users of wood, reaction wood is highly undesirable, because its mechanical properties are different from normal wood, making sawing difficult and often causing boards to twist or warp. In tendrils, g-fibres form a ribbon on the inside of the helix with increased lignification (strengthening) on the inner side. G-fibres are highly characteristic of mature tendrils, only forming after the tendril has finished attaching itself to a support. Coiling occurs because the inner and outer layers of the ribbon behave quite differently, especially as the tendril loses water, causing the inner layer to contract more than the outer layer. If the ribbon of fibres is extracted from the tendril, by dissolving the rest of the tendril using suitable enzymes, it retains its helical structure.

 Sticky climbers Darwin concluded his survey of climbing plants by mentioning root climbers and scramblers, but had little to say about either, and that rather neglectful attitude has tended to persist until quite recently. But we now 51

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know at least something about both; I’ll say more about scramblers (and one scrambler in particular) later, but let’s start with the recent surge in interest in the adhesive properties of ivy. As you can easily see, ivy attaches itself to walls and tree trunks via adventitious roots, that is, roots that develop directly from stems. This attachment is not a simple process.The key turns out to be root hairs, which are normally extremely delicate, short-lived structures involved in nutrient and water uptake from the soil. Ivy root hairs are quite different; they eventually become tough and lignified, but before that they insinuate themselves into tiny cracks and crevices in the surface of the support (on a perfectly smooth surface they show slightly different behaviour, but I think it’s safe to assume that ivy didn’t actually evolve to climb up glass or plastic). Each root hair has spirally arranged cellulose micro-fibrils, and as it dries it flattens into a spirally curled ribbon, eerily like the g-fibre ribbon of a cucumber tendril. This spiral contraction pulls the parent root towards the substrate and thus tightens the attachment. So, even though ivy’s climbing mechanism looks nothing like that of a tendril climber, there is remarkable convergence at the micro-scale. Not only does the basic cellular mechanism look the same, it operates in exactly the same way and performs the same function. 52

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Virginia creeper (Parthenocissus quinquefolia) showing a fully developed but young tendril, and an older tendril with the branches thickened and spirally contracted, and the extremities developed into adhesive discs. From Darwin’s book on climbing plants.

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But, before all this, the young root hair has to attach itself to the substrate, which it does by secreting glue. Darwin made some observations on the glue secreted by root climbers, chiefly of creeping fig (Ficus pumila), but also ivy, but made no real progress. It’s easy to see why; understanding how root climbers work awaited advances in microscopy and chemistry that weren’t available to Darwin. Not all glues work in the same way, but one underlying principle is extremely close contact between the two things you want to stick together, so that van der Waals forces (the weak forces between adjacent molecules) hold them together. This is the secret behind the ability of geckos to walk on the ceiling. The gecko’s feet are covered in millions of extremely tiny hairs, each further covered in hundreds of even smaller bristles. Each of these bristles makes intimate contact with the molecules of the ceiling, and the sum of the tiny electrostatic forces between them stops the gecko falling off. Ivy glue turns out to have much in common with geckos; it’s a nanocomposite composed of nanoparticles in a liquid polymer matrix, with the nanoparticles playing the part of the gecko’s bristles. The nanoparticles, which are 50–80 nanometres (billionths of a metre) across, are glycoproteins, although we’re still not sure exactly how ivy makes them. Nor are we sure exactly how they work; ivy glue is one of the strongest 54

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biological adhesives so far discovered, and about three times stronger than can be explained by van der Waals forces alone, so there are things going on that we don’t yet understand. Similar biological adhesives are used by mussels and barnacles to stick themselves – very firmly – to rocks. The ability to attach to a (more or less) flat surface clearly has advantages, and has evolved not only in several unrelated plant families, but also using very different structures. Ivy is a familiar example of a root climber, and we’ve already seen Darwin’s description of the adhesive tendrils of Virginia creeper. Both involve the secretion of some kind of glue. Another large family with many climbers, the Bignoniaceae (trumpet creepers), often have showy flowers and includes many species familiar to both temperate and tropical gardeners. Darwin studied the behaviour of several species and found them to be essentially grasping tendril climbers, although with many variations between species, so he was surprised to find that north American Bignonia capreolata (cross-vine) did something rather different: Finally, I may remark how singular a fact it is that a leaf should be metamorphosed into a branched organ which turns from the light, and which can by its extremities either crawl like roots into crevices, or seize hold of minute projecting points, these extremities afterwards forming cellular outgrowths which secrete an adhesive 55

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cement, and then envelop by their continued growth the finest fibres.

Fine tendrils that insert themselves into crevices, and can grasp any tiny projection, are common in the Bignoniaceae. In my own garden, Eccremocarpus scaber, the Chilean glory flower, manages every year to ascend each year a more or less flat wall. The rendering on the wall, with little more relief than coarse sandpaper, is apparently just rough enough for the plant to get sufficient grip to support itself. I say ‘just rough enough’, because my plant never looks entirely safe, and a summer storm is often enough to bring the whole thing tumbling to the ground. Cross-vine can clearly do something very similar, but has adopted the beltand-braces approach of also developing glue-secreting terminal pads, the whole eventually becoming strongly reminiscent of the adhesive tendrils of Virginia creeper. It’s easy to imagine – despite the achievements of my Chilean glory flower – that glue is an essential part of the trick of becoming firmly attached to a wall, or a cliff or tree trunk; all the most successful examples, including ivy, Virginia creeper and climbing hydrangea (Hydrangea anomala subspecies petiolaris) use glue. But apparently not, as a recent study of another member of the Bignoniaceae, monkey’s comb (Amphilophium crucigerum), demonstrates. The ends of the monkey’s comb’s tendrils start out like little grappling hooks, 56

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Monkey’s comb (Amphilophium crucigerum).

but once they encounter a rough surface, they develop attachment pads. The pad tissue develops to fill completely even the tiniest interstices and gaps within the substrate, then stiffens and strengthens, and the large contact area creates an effective friction-based anchoring system – without glue. 57

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 Darkness visible Twiners and tendril climbers are limited by the need to twine around, or grab hold of, something relatively narrow. As a result they tend to be confined to relatively well-lit environments, at least as youngsters, but the ability to climb up any vertical surface brings with it the opportunity to behave rather differently. In 1974 Donald Strong and Thomas Ray, from the University of Florida, set off for Costa Rica to study the climbing behaviour of the tropical root climber Monstera gigantea. That name is a bit ambiguous, so we aren’t sure which plant they studied, but it was clearly a species of Monstera, or in other words a sort of Swiss cheese plant. When Monstera seeds germinate on the floor of a tropical forest, where there is very little light, the seedlings have one overriding priority: to find the nearest tree and grow up it. To do that, they need to break the golden rule of nearly every other plant, which is always to grow towards the light. Instead Monstera seedlings grow towards the darkest place around, which of course is directly under the nearest tree, at which point their behaviour changes completely. In fact Monstera plants go through three distinct phases. Young seedlings, which grow very slowly in the prevailing gloom, have slender prostrate stems with tiny bract-like leaves.When the seedling meets a tree, which it detects by touch, it becomes attracted to light and changes to an ascending 58

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form with saucer-shaped leaves – at first only about 1 cm across, but later up to 25 cm in diameter. Only when the plant emerges into direct sunlight does it develop its characteristic adult foliage. Growing towards darkness is clearly adaptive for Monstera seedlings, but nevertheless, it’s a high-risk strategy, so Strong and Ray set out to find out how long the plants would persist with the strategy if it clearly wasn’t working. They set up a dark ‘cul-de-sac’, in the form of a box with three sides and a top, on the ground next to several seedlings, to see how far seedlings would grow into the dark. Seedlings dutifully grew towards the box but then stopped, and began growing aimlessly back and forth just inside the mouth of the box. The seedlings seem to switch to a positive response to light when the light grows very dim, but go back to preferring darkness when it’s a little brighter. As a result they became stuck in a state of permanent indecision when faced with the interior of a dark box – something natural selection never prepared them for. Many plants change their growth habit or leaf shape (or both) as they grow and mature, but it’s particularly common in climbers, perhaps because they often encounter quite different environments during their lives. Monstera is a nice example, and the different juvenile and mature leaf forms of ivy are well known, but there are more extreme examples, and it’s hard to 59

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Syngonium podophyllum – drawn by Adolf Engler in Volume 71 of Das Pflanzenreich (1920).

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beat Syngonium. Like Monstera, Syngonium is in the arum family (Araceae), and also germinates in the dim light of the tropical forest floor. The seedling starts off by producing a rosette of leaves, then produces a long slender stem with tiny leaves that heads off as usual towards darkness and the nearest tree. But unlike Monstera, it has a fail-safe strategy. If the shoot doesn’t run into a tree after about two metres, it then pauses and grows another leaf rosette, essentially establishing a new photosynthetic ‘base camp’, before setting off again with another searching stem. It can repeat this process indefinitely until it actually finds a tree to climb. The stem now climbs the tree, its leaves becoming larger and more complex in shape, just like Monstera, until it reaches the sun and flowers. But that’s far from the end of the story. At the top of the tree, the shoot continues to grow until it becomes detached from the tree and hangs down. As it grows down, its leaves again become smaller and less complex, until it hits the ground, whereupon it sets off for anything up to 20 metres, producing only tiny, widely spaced leaves. In this stage, the shoot pays no attention to light, but just travels in a straight line until it hits another tree, when it begins the ascending part of the cycle again. Presumably establishing new plants from seed is a chancy business, so Syngonium has found a way for the mature plant to bypass this stage and find new trees to colonise 61

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on its own. Many tropical climbers in the Araceae have adopted the same strategy. They are the classic creepers familiar to us all from Tarzan swinging across the jungle. Root climbers, or in fact any kind of adhesive climber, can afford to head for darkness, because they know that if they hit a tree trunk, they can use it as a support. Twiners need to be more careful, since most tree trunks will be of no use to them, but they would still like to find something to climb. How do they do that? Frankly, we don’t know, although American weed scientists, with a practical interest in how the weed ivy-leaf morning glory (Ipomoea hederacea) finds maize plants to climb, had a good try at finding out. They carried out a number of experiments, in both the field and greenhouse, in which young morning glory plants were given a choice of nearby maize plants and stakes painted black, bright red, light blue, light yellow, medium green, and white. The morning glories much preferred to climb maize, and they really didn’t like black, with the other colours somewhere in between.The researchers thought that the plants might be influenced by the total amount of light reflected by potential supports, or by the wavelengths of light reflected, but found no evidence for either hypothesis, and thus retreated, baffled. Morning glory obviously knows what it’s doing, even if we don’t know how it knows. 62

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 Chameleon vine I said that Syngonium was hard to beat when it came to the art of shape-shifting, but that was before the almost hallucinogenic abilities of the chameleon vine (Boquila trifoliolata; family Lardizabalaceae) were discovered in 2014. Chameleon vine is an expert mimic, changing its appearance as it climbs different hosts. If the host has long thin leaves, or short broad leaves, or tiny leaves, the vine has the same. If the host’s leaves are pale green, so are those of the vine. On a host with leaves with a mucronate tip (a small spine at the leaf tip), the vine has mucronate leaves too. It can’t quite manage serrated leaves, but does achieve leaf margins with a few random indentations. The same vine even changes leaf size and shape as it grows over more than one host. This causes obvious difficulties for plant identification; the official description of the vine is its ‘standard’ appearance when growing alone – which most of the time it looks nothing like. Two questions immediately arise: why, and how? ‘Why’ turns out to be surprisingly straightforward: there is some evidence that it helps to avoid herbivory. At least, compared to those growing on leafless branches, and therefore with nothing to mimic, vines growing among host foliage suffered less herbivore damage. ‘How’ is much less obvious, especially since none of the possibilities seems remotely plausible. Detection of 63

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A

B

C

D

E

F

Chameleon vine (Boquila trifoliolata). In each case, the dotted arrow points to the chameleon vine, and the solid arrow to the plant it is mimicking.

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volatile chemicals from the host seems highly likely, since plants are very good at this. But how has the vine learned that a particular smell goes with a certain leaf shape, size and colour? Horizontal gene transfer, i.e. somehow actually stealing a few genes from the host, suffers from the opposite problem – it might do the job, but how does it happen, in the right place and on the right timescale? This leaves us with some kind of vision, which really is uncharted territory. Observation has probably taken us as far as it can; we now need, for example, to see if the chameleon vine can still work its magic in darkness, which would soon check on the vision theory. In short, what we need are some cunning experiments; you can almost imagine Darwin doing them.

 Prickles and hooks Darwin clearly considered scramblers, which attach themselves to a support with the aid of prickles or hooks, to be the poor relations of the climbing-plant world; he devotes a mere two pages of his book to them. Even so, he managed to ask – and possibly answer – one interesting question. Noting that some climbing roses can ascend the walls of a tall house, if provided with a trellis, he mused: How this is effected I know not; for the young shoots of one such rose, when placed in a pot in a window, 65

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bent irregularly towards the light during the day and from the light during the night, like the shoots of any common plant; so that it is not easy to understand how they could have got under a trellis close to the wall.

In other words, how does a rose become, and remain, attached to a trellis on a wall if it grows towards the light, and thus away from the wall? Darwin then answers his question in a footnote. His friend and correspondent Asa Gray, widely regarded as the pre-eminent American botanist of the nineteenth century, had observed that ‘the strong summer shoots of the Michigan rose (Rosa setigera) are strongly disposed to push into dark crevices and away from the light, so that they would be almost sure to place themselves under a trellis’. He adds that ‘the lateral shoots, made on the following spring, emerged from the trellis as they sought the light’. So it looks like ‘climbing’ roses, rather like the climbing Araceae mentioned above, have adjusted their response to light to make sure they can find and hang on to a support – but once they’ve done that, they grow towards the light as usual. More or less in passing, Darwin mentions Galium aparine (goosegrass or cleavers), probably the commonest and most familiar scrambler in the British flora. He obviously thought that there was nothing much to say about it, but recent research has shown that this undistinguished weed is cleverer than you might think. 66

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Goosegrass, as you may well have accidentally discovered, is covered in hooked trichomes or hairs, which allow it to stick to socks and sweaters like botanical Velcro. But goosegrass did not evolve to stick to socks; so how does it work? Well, the work is mostly done by hooks on the leaves, which are different on the upper and lower surfaces. The hooks on the upper surface bend forwards, towards

Goosegrass (Galium aparine), showing the arrangement of hooks on the upper and lower surfaces of the leaves.

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the tip of the leaf; those on the lower surface bend towards the base of the leaf; they’re much tougher too. The effect of the hooks on the upper surface is to largely prevent leaves ending up below the leaves of the support, and those that do easily slide out again. But the tough, backwardly directed hooks on the lower surface act like grappling hooks, firmly attaching the leaves to the upper surfaces of the leaves, stems and even flowers of the host. As the host and the goosegrass both move around in the wind, the result is a ratchet effect; goosegrass leaves easily slide out from under the leaves of its host, but those on top slide further over and cannot be withdrawn, resulting in an ever closer and more secure attachment. Thus goosegrass ends up with its leaves exactly where it wants them to be – firmly fixed above the leaves of its support. So effective is this ratchet that the whole plant risks being torn out of the ground. To counter this the lower parts of the goosegrass stem are both unusually extensible and can withstand an unusually high strain before breaking – in fact goosegrass appears to be something of an engineering marvel, although how it does either of these things is unknown.

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CHAPTER 2

Slow Learners The power of movement in plants (1880)

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owards the end of his life, and in one of his last major works, Darwin returned to plant movement in his book The Power of Movement in Plants, which he wrote together with his son Francis (later to become an eminent botanist in his own right). One motivation was his genuine fascination with the whole subject of plant movement; another was his continuing attempt to address critics of The Origin of Species. Much of The Origin is taken up with showing that natural selection proceeds by the accumulation of small modifications of existing structures or behaviours that confer some selective advantage, however small. Here is one key passage: Mr. Mivart is further inclined to believe, and some naturalists agree with him, that new species manifest 69

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themselves ‘with suddenness and by modifications appearing at once’. For instance, he supposes that the differences between the extinct three-toed [horse ancestor] Hipparion and the horse arose suddenly. He thinks it difficult to believe that the wing of a bird ‘was developed in any other way than by a comparatively sudden modification of a marked and important kind;’ and apparently he would extend the same view to the wings of bats and pterodactyles. This conclusion, which implies great breaks or discontinuity in the series, appears to me improbable in the highest degree.

And later in the same passage, in case he hadn’t made himself clear enough: To admit all this [Mivart’s ‘prodigious transformations’] is, as it seems to me, to enter into the realms of miracle, and to leave those of science.

The Mr Mivart that Darwin refers to here is St George Jackson Mivart, one of Darwin’s fiercest opponents, writing in his 1871 book The Genesis of Species. Some of Mivart’s objections referred specifically to Darwin’s work on climbing plants; one of the many things that Mivart didn’t believe could have arisen gradually was climbing in plants, and proving him wrong was one of the motivations behind Darwin’s return to the subject of plant movement in his 1880 book. One of Darwin’s favourite techniques was to overwhelm potential critics with a mountain of 70

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empirical evidence in support of his ideas. One of the problems with this approach was that it did tend to slow things down – no-one could accuse Darwin of jumping to hasty conclusions. Darwin famously wrote a short sketch of his theory of natural selection in 1842, enlarging it during the summer of 1844 into one of 230 pages. But he then continued to pile up supporting evidence, which was why it was still unpublished when Alfred Russel Wallace turned up with the same idea in 1858. So similar were the two men’s theories that Darwin wrote ‘if Wallace had my MS sketch written out in 1842, he could not have made a better short abstract!’ In the end a joint presentation was made to a meeting of the Linnean Society of London on 1 July 1858. Unlike Darwin, Wallace did not let the grass grow under his feet; the idea of natural selection had only come to him in February 1858, during an attack of fever on a remote Indonesian island. Darwin’s panic at the sight of Wallace’s essay can be judged from the fact that the Linnean Society presentation took place only fourteen days after the essay’s arrival in England. The power of movement in plants is a fine example of the Darwin method in action. He repeated the same experiments over and over, using a wide range of species; this doesn’t make the book much of a pageturner except to engender in the reader a profound 71

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desire to get to the end. Darwin himself, correcting the proofs, remarked that the book was a ‘horrid bore’, and he frankly encouraged his readers to skip most of the book and go straight to the summary in the last chapter. It is, as ever with Darwin, excellent advice. In support of his gradualist ideas, Darwin proposed that twining, the simplest form of climbing, evolved from the modification of behaviour shared by all plants. Darwin proposed that in all plants the growing tip bends successively to all points of the compass, so that the tip revolves. This movement has been called by Sachs “revolving nutation”; but we have found it much more convenient to use the terms circumnutation.

It follows that climbing is a natural development of circumnutation: Thus, the great sweeps made by the stems of twining plants, and by the tendrils of other climbers, result from a mere increase in the amplitude of the ordinary movement of circumnutation.

Darwin started out by showing that all parts of the plant exhibited circumnutation, and that this began immediately after germination of the seed; he suggested that it initially arose to help the seedling root penetrate the soil, avoiding stones along the way, and to help the young stem to emerge from the soil.Thus, since all the growing parts of a plant are constantly in motion, it is a short step to more directed, purposeful forms of movement. One 72

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of these is a response to light, and here Darwin made observations that were – much later – to have a profound impact on the whole science of plant biology. Darwin first noted that with few exceptions, all plants are very sensitive to light and will always grow towards it. He then noted that the seed leaf (or coleoptile) of a grass seedling is exceptionally sensitive to even tiny amounts of light, presumably because of the extreme importance of light ‘as a guide from the buried seeds through fissures in the ground or through overlying masses of vegetation, into the light and air’. He therefore settled on the coleoptiles of seedlings of reed canary grass (Phalaris canariensis) as a convenient experimental system. He then made a crucial observation: Whilst observing the accuracy with which the cotyledons of this plant became bent towards the light of a small lamp, we were impressed with the idea that the uppermost part determined the direction of the curvature of the lower part. When the cotyledons are exposed to a lateral light, the upper part bends first, and afterwards the bending gradually extends down to the base, and, as we shall presently see, even a little beneath the ground.

This led in turn to the conjecture that there was something special about the upper part of the coleoptile. But what was it? Did the upper part have to bend before the lower part was able to do so? But no – if the upper 73

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part was enclosed in a narrow glass tube, or fixed to a tiny splint, and thus unable to move, the lower part still bent towards the light. Next he tried surgery; if anything from 2.5 to 4 mm was cut off the top, the rest of the coleoptile did not bend. But if only a little over 1mm was removed, bending was reduced, but still took place. It was still possible that such injury removed the ability to bend, rather than the ability to perceive the light, but another experiment soon solved that. Coleoptiles fitted with opaque tin-foil caps, or short black-painted glass tubes, did not bend, even if most of the coleoptile was still fully exposed to light. Finally, if the upper parts of coleoptiles were painted with Indian ink on one side only, they bent towards the unpainted side, even if this was not directly facing a window.

Intact seedling (curvature)

Tip of coleoptile excised (no curvature)

Opaque cap on tip (no curvature)

Buried in fine black sand but with extreme tip left exposed (curvature)

This (highly simplified) diagram summarises some of Darwin’s 1880 experiments on the response of grass seedlings to light.

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As Darwin noted, these experiments led inescapably to one conclusion: ‘These results seem to imply the presence of some matter in the upper part which is acted on by light, and which transmits its effects to the lower part.’ It’s hard to exaggerate the importance of Darwin’s experiments. For one thing, they established grass coleoptiles as the go-to system for many basic investigations of plant physiology, as they still are to this day (in much the same way that the fruit fly Drosophila became the model organism for animal genetics). Darwin’s work also led directly to the discovery, fifty years later, of the plant hormone auxin. How auxin works, how it mediates the effect of light on growth, and the nature of the photoreceptor involved, have been major research topics in plant biology throughout the twentieth century and into the twenty-first. But more than that, Darwin’s work contributed to the end of the prevailing orthodoxy of preceding centuries, which was that plants were dull pieces of machinery, without sense or sensitivity. According to this view, if plants responded to the environment at all, that response was a mere direct mechanical effect. Thus if roots grew downwards, they were responding to gravity with no more sense of purpose than Newton’s apple falling from the tree; if a stem bent towards the light, that was only because the light speeded up maturity (and thus 75

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cessation of growth) of the lit side, or simply dried out the illuminated cells so that they grew more slowly than the dark ones. But Darwin showed that plants were able to perceive a stimulus, which then caused a different part of the plant to react in a specific and clearly adaptive way. The parallel with animals was clear to Darwin: ‘There is therefore no improbability in this power having been specially acquired. In several respects light seems to act on plants in nearly the same manner as it does on animals by means of the nervous system.’ The seed of the idea that plants can think had been sown.

 Lean on me A plant’s innate movements are modified by responses to the environment, and the two great influences are light and gravity. As we’ve just seen, Darwin carried out groundbreaking research on the response of plants to light. Gravity wasn’t so easy to work with, as Darwin ruefully acknowledged (‘it is impossible to modify in any direct manner the attraction of gravity’); in fact it’s only with the advent of space flight that we’ve been able to modify gravity in a way that no earth-bound observer can hope to do. Nevertheless Darwin was able to show that, just as light acts on the tips of shoots, gravity acts on the tips of roots, although this causes other parts of the root to bend: ‘we now know that 76

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it is the tip alone which is acted on, and that this part transmits some influence to the adjoining parts, causing them to curve downwards.’ Light and gravity usually operate in opposition; organs that respond positively to one generally respond negatively to the other. So, as Darwin noted, however much a plant may be pulled this way and that by light during the day, gravity is always there to restore the natural order at night:‘When the stem of any plant bends during the day towards a lateral light, the movement is opposed by apogeotropism [bending in opposition to gravity, away from the centre of the earth]; but as the light gradually wanes in the evening the latter power slowly gains the upper hand, and draws the stem back into a vertical position.’ Thus gravity wins in the end; it may seem almost too obvious to remark, but plants tend to be vertical, even as we move a long way from the equator and light comes more and more from the side. Nowhere is this vertical growth more obvious than in the case of trees, where the mechanical disadvantages of leaning are selfevident; indeed if we see a leaning tree, we generally assume it’s in some kind of trouble. Trees have therefore evolved elaborate self-righting mechanisms that detect and respond to any tendency to lean. Interestingly, although this always involves the growth of ‘reaction wood’ in response to the asymmetric forces generated 77

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Cook pines (Araucaria columnaris) in California, defying gravity as they lean heavily towards the equator.

by leaning, the exact mechanism isn’t always the same; in hardwoods tension wood is formed on the upper side of a tilted stem, while in softwoods compression wood grows on the lower side. But the world is full of surprises, and there is – remarkably – one leaning tree. Araucaria columnaris (Cook pine) is endemic to the remote island of New Caledonia, but is widely cultivated in warm temperate 78

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climates throughout the world. Not only does Cook pine lean, it always leans towards the equator, and furthermore its lean increases as it gets further from the equator. In short, although we have no idea why, Cook pine looks like the one tree where gravity has not gained the upper hand. Like its close relative, Norfolk Island pine, Cook pine is too frost-sensitive to grow beyond 40º north or south. But unlike Norfolk Island pine, one can’t help wondering if a contributory factor is that Cook pines that ventured any further north or south would simply fall over. In The power of movement in plants, Darwin scarcely mentions trees, since he clearly found that herbaceous plants provided the most amenable experimental material. On the rare occasions he experimented on trees, they were seedlings or very young plants. It’s also very unlikely that he was aware of the existence of Cook pine, which is much too tender to grow outdoors in Britain, struggling even on Tresco. But knowing what we do now, you can’t help thinking that he would have loved to get his hands on one.

 Mimosa pudica A curious feature of The power of movement in plants is what Darwin chose, apparently almost perversely, not to talk about. The leaves of the sensitive plant, Mimosa pudica, are remarkably sensitive to touch. Darwin knew 79

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this, of course, but mentions it only in passing: ‘the cotyledons of Mimosa pudica being only slightly sensitive [to touch], whilst the leaves are well known to be so in the highest degree’. Later, he says ‘This plant has been the subject of innumerable observations’; perhaps the unspoken comment being that he would leave others to add to the existing mountain. Darwin was right about the interest in Mimosa; it’s one of those plants, like the Venus fly-trap, that everyone has heard of, and nearly everyone can get excited about. It had even come to the attention of Charles II, who directed the newly formed Royal Society to explain its movements. A special committee was established, which conducted experiments that showed that the size of the plant’s response depended on the magnitude of the touch. Most of the committee were physicians, much taken at the time with William Harvey’s relatively recent discovery of the circulation of the blood, so it’s not surprising that the theory they came up with postulated the existence inside the plant of an ambiguous circulating liquor or spirit. The plant’s ability to move was somehow linked to the movement of this – quite imaginary – spirit. Essentially they seemed to think that if a plant could move, it must be well on the way to being an animal. For those who have never seen one, Mimosa pudica has compound leaves, with two or four leaflets, each 80

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further divided into numerous narrow segments or pinnules. When the leaf is touched, the pinnules fold up, like closing a book. This kind of thing happens at night in many plants, and Darwin devoted a large part of The power of movement in plants to investigating such ‘sleep movements’. The unusual thing about Mimosa is the speed of this movement – it takes less than a second to start, and is more or less finished after about 4–5 seconds. At the same time, the whole leaflet droops downwards from its normal horizontal state, sometimes ending up almost vertical. It’s generally assumed to be an anti-herbivore adaptation; you can imagine that an insect might be dislodged by such rapid movement, and a vertebrate herbivore that wasn’t paying close attention might think that the plant had simply disappeared.

A sensitive plant: Mimosa pudica leaf in its open and closed state.

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The key to such rapid movement is that a sensitive plant leaflet is closed or folded in its ‘resting’ state, and is only maintained in the ‘open’ state by hydrostatic pressure, the plant pumping water into the pulvinus or ‘hinge’ at the base of each pinnule, thus forcing the leaflet erect. Following a stimulus, the plant opens pores that allow this water to pour out of the cells, causing the leaf to collapse back to its closed, resting state. The paradox, of course, is that what looks like a very ‘active’ movement is really quite passive, merely involving the leaf or trap returning to its natural state. Interest in Mimosa has not abated with time, and recently Mimosa has played a key role in the debate about just how clever plants really are. For example, we know that touching or stroking the leaves of Mimosa causes them to rapidly fold up. This is very animal-like behaviour: give an animal a stimulus that elicits some kind of defensive reaction, and you get the reaction. But what happens if you keep on doing it? The animal soon learns that nothing bad happens, so stops responding. This lack of response is called habituation, and it allows the animal to focus on the important things in its environment, while filtering out things that repeatedly turn out to be irrelevant or innocuous. Mimosa does exactly the same. It responds to a single touch or shock, but soon learns not to bother if you

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keep poking it; it will start to reopen its leaves very quickly after folding them, and eventually it gives up folding altogether. But of course that in itself is not very good evidence of memory, or learning, or much at all; maybe Mimosa leaves just stop responding because they become tired? In fact we can show that Mimosa doesn’t just stop reacting because it’s tired. If you give it a new, different stimulus (a good shake, say, rather than a poke), it responds with the usual defensive leaf folding. But then give it the original stimulus again: nothing. That’s real learning for you: ignoring the original stimulus, but not being fooled into ignoring a new one. Further evidence that Mimosa is cleverer than you think comes from experiments in which the light level is varied. Leaf-folding, as a strategy to fool herbivores, has to be balanced against its negative effect on photosynthesis, which is nearly halved in folded leaves. Therefore Mimosa is quicker to ignore a recurrent, but harmless, stimulus when grown in dim light, in other words when the need to keep leaves fully open is more urgent. Moreover, Mimosa remembers to ignore the stimulus for longer in dim light, for exactly the same reason, and this memory persists for at least a month. And all this without a brain, or a nervous system of any sort.

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It would be easy to get the idea from all this that Mimosa is some kind of genius, a veritable Einstein among vegetables. But there’s no evidence for this at all. The reason all this work has focused on Mimosa is simply that its ability to move (and fast) makes it a convenient experimental subject, which in turn reveals just what a hasty bunch we are; other plants may well be smarter than Mimosa, but until very recently biologists had generally decided that it would take too long to find out. One of the very few who has had the patience to study plant intelligence is an Australian botanist called Monica Gagliano, whose latest work shows that peas are at least as smart as Mimosa.We all know that animals can easily learn to respond to a stimulus associated with a reward; Pavlov trained dogs to associate food with the sound of a metronome, so that eventually they started to salivate merely at the sound. We tend to think that this kind of associative learning is confined to animals, but Gagliano has shown that plants do it too. If pea shoots are ‘trained’ to associate air movement from a fan with light, they soon learn to respond to the fan alone, in the absence of light. What’s more, the training only works if it happens during the day; you can’t fool a plant into associating a stimulus with light at night, because millions of years of evolution have persuaded plants that there’s never any light at night. 84

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 Plant intelligence Darwin may not have had much to say about Mimosa, but he did have something to say about plant intelligence. Indeed, in what may be the most prophetic sentence he ever wrote, at the very end of The power of movement in plants, he says: It is hardly an exaggeration to say that the tip of the radicle [root] thus endowed, and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements.

Darwin saw clearly that although plants are literally brainless, that doesn’t make them stupid. In fact we worry about brains only because we have brains. Plants don’t have lungs either, or a liver, or kidneys, but they carry out the functions of those organs, so why can’t they think without a brain? What Darwin is saying in the quote above is that plants appear to have a ‘distributed intelligence’, in which every part of the plant cooperates in processing information and making decisions; every plant has its own personal ‘internet’, much of it below ground. In fact plants are constantly monitoring the environment around them and taking whatever action is necessary. Roots in soil are aware of other nearby roots, and moreover they know whose roots they are. 85

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So was Darwin right? Are plants intelligent? Swiss psychologist Jean Piaget described behaviour as: ‘all the actions directed toward the outside world in order to change conditions therein or to change their own situation in relation to these surroundings’. Clearly that applies to plants. Plants display an intentional, purposeful ability to solve problems, and that’s as good a definition of intelligent behaviour as any. As molecular biologist Anthony Trewavas puts it:‘Plants that can place a root or shoot in the best position to gain resources, as against indifferent or resource-absent places, act intelligently. Those plants that most quickly estimate which branches or leaves no longer provide adequate resource-gathering potential and block them from further root resource access, have a higher capacity for problem solving. Those plants that more accurately predict the future resource availability or herbivore damage and decide on resource distribution appropriately are smarter than others, and the reward is a likely gain in fitness.’ The only reason we don’t think plants are very clever is that we associate awareness, and even intelligence, with movement, and plants – with very few exceptions – move too slowly for us to notice. As German plant physiologist Wilhelm Pfeffer commented in 1906: The fact that in large plants the power of growth and movement are not strikingly evident has caused plants

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to be popularly regarded as still life … If mankind from youth upwards were accustomed to … perceive the activities of weeks or months in a minute as is possible by the aid of a kinematograph, this erroneous idea would be entirely dispelled.

The debate about plant intelligence is largely a twentyfirst-century phenomenon. Darwin, far ahead of his time as usual, understood that plant intelligence is so unlike the human variety that we simply fail to recognise it. As Stefano Mancuso points out in his little book Brilliant Green, we wouldn’t recognise a really alien intelligence if we tripped over it, and the search for intelligence in outer space is merely a search for ‘our own intelligence, lost somewhere in space’. If we deny that plants are intelligent, all we really mean is that they aren’t like us.

 Helianthus annuus Considering how much of it is devoted by Darwin to circumnutation, and to the various ways in which plants respond to light, another startling omission from The power of movement in plants is the great sunflower rotation mystery. A piece of natural history that appears to be well known to just about everyone is that sunflowers turn to follow the sun as it moves across the sky. Or do they? Plenty of people must think so, because some of the sunflower’s names in other languages refer directly 87

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to this behaviour, e.g. girasol in Spanish and tournesol in French. Yet Gerard, in his famous 1597 Herball, was having none of it: ‘some have reported it to turn with the sun, the which I could never observe, although I have endeavoured to find out the truth of it.’ We now think we know why Gerard was confused; immature sunflower heads follow the sun, but once the flowers mature and start to shed pollen, they settle down and face east for the rest of their lives. But others were confused too, and the sunflower’s daily rotation was only finally established beyond doubt (with photographs) in the 1890s. But that’s only the start; why do they do it? A team of American botanists recently reviewed the evidence and concluded that, frankly, no-one really knows, although there’s no shortage of hypotheses. For example, Darwin provided plenty of examples of plants with leaves that follow the sun, and such behaviour definitely increases photosynthesis. So flower turning may just be an accidental side effect of the fact that the leaves, or maybe even the photosynthetic bracts beneath the head itself, like to face the sun. Alternatively, the main reason may be the maintenance of a higher and more constant temperature, perhaps helping to attract more pollinators or speed up seed development. And when rotation stops,why do sunflowers always end up facing east? Again, there are somewhat contradictory 88

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A field of sunflowers in California, all facing the sun.

hypotheses. Maybe facing east in the morning dries out the morning dew and reduces the possibility of fungal infection. Or possibly, like the rotation itself, more rapid warming in the morning is all about attracting more pollinators. Alternatively, perhaps facing east helps to keep the flower cool on hot afternoons (pollen grains in particular don’t like to be too hot). One problem is that most researchers have studied sunflowers cultivated for oil or for ornament, but the 89

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turning behaviour presumably evolved in their wild ancestors, which are very different plants, much more branched and with much smaller flowers. Perhaps we need to pay more attention to these wild ancestors. When it comes to the how rather than why, we know a bit more; for a start, a moving light source is essential. Sunflowers don’t turn if you raise them in a room with stationary, overhead lighting. But at least part of the daily cycle doesn’t need light, because sunflowers turn back to face east at night, and in fact this movement is about twice as fast as the daytime motion. And once they get started, sunflowers tend to stick with the same routine. If you confuse a sunflower by rotating it through 180º at night, it carries on regardless, only re-coordinating with the sun after several days of facing the wrong way. It also doesn’t look like the flower itself is all that important; if you decapitate a sunflower, the stump continues to turn. But leaves are necessary – remove them and movement stops. Not just any old leaves, either; movement ceases if you remove the mature leaves, but starts again when young leaves reach maturity. If we look at ‘how?’ in more detail, sunflowers present us with a lifetime’s worth of interesting questions. For sunflowers must at least (1) during the day, be capable of detecting the presence and direction of a light source; (2) translate this perception into differential growth of different sides of the stem, carefully coordinated with 90

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the east-to-west movement of the sun throughout the day; (3) know how and when to throw all this growth into reverse, so that the flower, like Cinderella’s coach, gets back to where it should be before sunrise; and last but not least, (4) stop all this movement when the flowers in the head mature. The first question was more or less solved by Darwin’s ingenious grass coleoptile experiments. Interestingly, sunflowers and coleoptiles both respond to blue but not red light; Darwin seemed to think this common knowledge, noting without comment ‘light from a paraffin lamp passing through a solution of bichromate of potassium [i.e. red light], which does not induce heliotropism’.The receptors are now known as phototropins, but they were not finally identified until the 1990s. Prime candidate for the differential growth in response to light is the ‘matter’ that Darwin speculated caused the same behaviour in grass coleoptiles, i.e. auxin. Auxin certainly seems to be responsible for increased growth of the shady side of the plant, but the exact mechanism may not be the same; in the former it seems to be transport of growth-promoting auxin from illuminated areas into shaded areas of plants, but the latest evidence from sunflowers implicates the generation of auxin inhibitors in illuminated tissues. Question (4) looks like the simplest of the lot, and maybe it is, but we still don’t know exactly why the head 91

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stops turning. Maybe the signal is simply switched off, or maybe new and unknown signals, possibly produced by the mature head, actively repress lateral stem growth. Maybe it’s a simple mechanical effect; to support the increasingly weighty head, the cells just get tougher and less flexible. More than one PhD thesis awaits this simple question alone. Question (3) is the one we know by far the least about. The nature of the rapid movement back to the east by dawn, and the fact that it continues even if the plant is experimentally confused, strongly suggest the presence of a circadian clock (from the Latin circa, ‘around’, and diem, ‘day’), i.e. some kind of innate molecular timekeeper operating on a period of about 24 hours. Circadian clocks, which are found in all forms of life, make sure that the organism is primed to respond to predictable environmental variation (e.g. night and day) in the right way at the right time. The exact nature of the sunflower circadian clock remains unknown. In particular, we don’t know whether the same clock operates in opposing directions at different times of day, bending the stem one way during the day and another at night. This kind of differential operation of a circadian clock within the same organ is otherwise known only from the mammalian brain, and not from plants at all, so finding it in sunflowers would be a bit of a game changer. 92

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Naturally enough, Darwin doesn’t mention circadian rhythms in The power of movement in plants; its serious scientific investigation didn’t begin until the end of the nineteenth century, and the actual term was only coined in the 1950s. But he was aware that many of the plants he studied exhibited daily rhythms; towards the end of the chapter on ‘sleep’ movements in plants, he observes: As the leaves of most plants assume their proper diurnal position in the morning, although light be excluded, and as the leaves of some plants continue to move in the normal manner in darkness during at least a whole day, we may conclude that the periodicity of their movements is to a certain extent inherited.

Moreover, Darwin was sure that these rhythms were not simply direct responses to a changing environment, for in a footnote he adds: Pfeffer denies such inheritance; he attributes the periodicity when prolonged for a day or two in darkness, to ‘Nachwirkung,’ or the after-effects of light and darkness. But we are unable to follow his train of reasoning.

In short, German plant physiologist Wilhelm Pfeffer thought plants were passive machines, but Darwin thought they were smarter than that, and as usual he was right. Finally, before we leave sunflowers, one last question: what exactly is a sunflower doing as it turns? Well, one thing it isn’t doing is actually turning, any more than 93

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the stem of a climbing twiner twists; all that happens is that the shaded side of the stem below the head grows faster than the illuminated side. So rather than rotating, the flower is better described as tilting towards the sun.

 Fast and furious As we’ve seen, Darwin didn’t say much didn’t say much about Mimosa pudica, and even less about sunflowers. But he could have done, and I’m still a bit surprised that he didn’t, if only because some of the experiments involved are so very Darwinian. I can just picture him getting up in the night to confuse his sunflowers by turning their pots round. On the other hand, other aspects of the study of plant movement have advanced in ways that Darwin could scarcely have imagined, often driven by technologies that simply weren’t available to Darwin. It’s instructive to look at a few examples.

 The fern sporangium: a cavitation catapult When it comes to movement – or rapid movement, at least – plants face all kinds of problems. Not the least is that, as everyone learns in Biology 1.01, the distinguishing feature of plant cells is that each is surrounded by a rigid cellulose cell wall, which is why the existence of cells was first recognised in plants. This, aided by other even tougher compounds in large plants, and with the help of some turgor (hydraulic pressure) in smaller ones, is 94

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what keeps plants upright. It’s a great system, cheap to construct, extremely tough, and capable of building enormous structures – as long as you don’t need to move. So not only do plants not have muscles, it wouldn’t do them much good if they had, because muscle cells need to change shape, and the rigid cell wall prevents that. But as long as we approach the problem in the right way, that rigid box around every plant cell is not part of the problem, it’s part of the solution.The cell wall allows plants to slowly store elastic energy, and then rapidly release it.We long ago discovered how good plants were for this. The English longbow, the dominant European battlefield weapon for two centuries between 1250 and 1450, relied entirely on the energy stored by bending a piece of wood. The amount of energy stored by a longbow was colossal, limited only by the strength and training of the archer. The best archers started young, graduating from smaller to larger bows as they grew up, and skeletons recovered from Henry VIII’s flagship the Mary Rose reveal how using a longbow resulted in obvious skeletal modifications. It would be surprising if plants hadn’t found their own ways of exploiting the possibilities of rigid plant tissues for storing, then rapidly releasing, large amounts of energy, and they have. One of the best examples is the fern leptosporangium. Ferns are primitive plants that reproduce by spores, which are tiny and very light, so once they get airborne, 95

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they can travel vast distances on the wind. But it’s that initial step that’s the problem. Some kind of launch mechanism is required, a problem that ferns have solved with one of the most elegant bits of machinery in the plant kingdom. The sporangium is tiny, and wrapped part of the way around it is the annulus, a strip of cuboid cells. In a dry environment, these cells lose water and shrink. Or at least they try to shrink; this attempted shrinkage is converted into bending because the cell walls have U-shaped thickening, thin on the outer face and thick on the others. This backward bending slowly straightens out the annulus like stretching back a catapult, breaking open the sporangium and gradually building a high negative pressure within the annulus cells. When this negative pressure reaches a critical value, cavitation occurs in the annulus cells, i.e. bubbles are formed, releasing the tension and causing rapid cell expansion. This flings the spores out at up to 10 metres per second, briefly exposing them to about 100,000g; forces that would squash you or me like a pancake (but fortunately spores are much tougher than people). The whole operation resembles the action of a medieval siege catapult. The mechanism as described is clever enough, but recent work has unearthed even more detail of exactly how it works. If that’s all the annulus did, when the tension was released it would simply snap shut and 96

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A fern leptosporangium in action. Note the annulus cells with their U-shaped thickening.

the spores would be back where they started. Builders of medieval catapults knew this, which is why such weapons all have a crossbar that stops the motion of the arm midway. Thus the arm is suddenly arrested, but the projectile continues; without the crossbar, the catapult would simply slam the projectile into the ground. Sporangia, obviously, don’t have a crossbar, so how do they work? 97

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We now know that the sporangium closes in two phases. In the first phase, the elastic energy stored in the cell wall is converted extremely rapidly into kinetic energy, and the sporangium partly closes (by 30–40 per cent) in about 1/100,000 of a second, one of the fastest movements ever recorded, in plants or animals. It’s this partial closure that launches the spores. During this extremely rapid first phase, water trapped in the cell walls has no time to escape, so pressure builds up, briefly blocking the return of the annulus to its original position. In the second phase, which is still very fast (a few hundred milliseconds), but much slower than the first, this pressure slowly relaxes as water flows through the cellulose matrix of the cell wall, allowing the annulus to close completely.The two phases are crucial, with the deceleration midway allowing the spores to be launched while the annulus is still open. One can only be impressed that a single row of twelve or thirteen cells can reproduce all the functions of a medieval catapult, including the power source, a triggering mechanism, and a means of briefly arresting the return to the closed position. Darwin would have loved all this, but the fine detail of exactly how the fern sporangium works was only discovered in 2012, and relied on a high-speed camera capable of thousands of frames per second, followed by digital image analysis. 98

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 Re-usable movement: horsetail spores The fern sporangium is an example of the ‘one-shot’ approach to movement. Naturally enough; it’s designed to launch the spores into the air, and once they’re launched, they don’t need launching again. Not only that, an easy way to trigger the release of a ‘single-use’ mechanism is some kind of fracture, so once the launcher is used, it’s broken, just like an opened soft-drink can. But there are plenty of examples of rapid movement in plants that use structures that can be used over and over. For example, horsetails, like ferns, although not very closely related to them, are primitive vascular plants that reproduce by spores. In stark contrast to the elegant ballistic machinery of ferns, horsetail sporangia don’t do much at all; they’re just bags of spores.The magic lies in the spores themselves, each of which has four ribbon-like structures attached called elaters. Each elater has a tough, waterproof side and a more elastic, hygroscopic side that expands and contracts as it absorbs and loses water. The result is that when the spore is wet, the elaters are tightly coiled around the spore, but as the spore dries they unfurl, until a dry spore looks like a spider with half its legs missing. This coiling and uncoiling, which is fully and rapidly reversible, helps the spores to spill out of the sporangium, and once on the ground, allows them to ‘walk’ around. Sometimes, spores get tangled up together in small clusters of five or six, and such clusters take somewhat larger ‘steps’ than 99

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A horsetail (Equisetum) spore, with its elaters tightly coiled (top right) when wet and unfurled (bottom) when dry.

single spores. But none of this gets them very far, and they always run the risk of walking around in circles and ending up back where they started. But the elaters can do more than that; when a spore is wet, its elaters can become tangled up. As the spore dries they at first remain tangled, even though the 100

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drying means they would like to straighten. Eventually this tension is released as the elaters abruptly straighten, releasing their energy like the sudden uncoiling of a spring, propelling the spore up to 1 cm into the air at up to 1 metre per second. That may not seem like much, but for an object less than 0.005 cm across, it’s an immense distance, the equivalent of a human leaping over the Shard, with a few feet to spare. The jump itself, of course, doesn’t move the spore very far, but it’s enough to boost the spore up into the breeze, the first step on the way to genuine long-distance dispersal. And like the short-range ‘walking’, the jumps are indefinitely repeatable, so a spore can just keep on jumping until it does make its escape.

 Nuytsia floribunda Fern sporangia and horsetail spores are examples of very rapid movement, albeit on a very small scale. But movement doesn’t have to be fast or microscopic to be surprising. Nuytsia floribunda, the Western Australian Christmas tree, grows in Southwest Australia, where the dry climate and some of the poorest soils on earth have led to a proliferation of plants with unusual ways of making a living, including a remarkable diversity of parasites and carnivores. Nuytsia is a hemiparasite, which means that it looks like a normal plant above ground, but below ground it parasitises the roots of other plants. 101

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All root parasites produce haustoria that attach to the roots of the host, but the haustorium of Nuytsia is, as far as we know, unique. It grows a pair of botanical ‘scissors’ with two sharp, sickle-shaped blades. A fluid-filled gland develops a hydrostatic force that pushes the two blades together, neatly amputating the host root, and Nuytsia then simply plugs its own vascular system into that of the host. Roots of up to 15 mm in diameter can be severed in this way. Everything about Nuytsia challenges your beliefs about what plants can and can’t do. The blades of the ‘sickle’ are extremely sharp, and will cut not only paper, but also human skin if you’re not careful. The whole root-amputation process is remarkable; when researchers dug up and examined over 400 haustoria, they intercepted only five of them in the act of cutting their way through a root, suggesting that it happens very quickly. And Nuytsia is not at all particular about its host. It will attach to any root that it encounters, and has even been known to cut through plastic-coated underground cables, to the dismay of telecommunications companies who have had to resort to using cables with extra-thick coverings.

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CHAPTER

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The Biter Bit Insectivorous plants (1875)

I

t is almost too obvious to need saying, but plant carnivory is not like animal carnivory; it exists for a fundamentally different reason. For carnivorous animals, their prey is fundamentally a source of fuel – of energy and calories. For carnivorous plants, the prey is a source of minerals, especially nitrogen and phosphorous. Although there are exceptions, most carnivorous plants, as we shall see, generally live in welllit places. And despite often being somewhat inefficient at photosynthesis, they still manage to fix lots of CO2 and do not need to kill to eat in the normal sense. Darwin knew this, of course, observing of sundew: Considering the nature of the soil where it grows, the supply of nitrogen would be extremely limited, or quite deficient, unless the plant had the power of obtaining this important element from captured insects. 103

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The sundews themselves, Darwin noted, know what’s good for them: the results of placing drops of various nitrogenous and non-nitrogenous organic fluids on the discs of leaves were given, and it was shown that they detect with almost unerring certainty the presence of nitrogen.

In fact Darwin seemed to understand the ecology of carnivorous plants perfectly. This may not seem surprising, but we should recall that he was writing at a time when the idea that carnivorous plants derived any benefit at all from their captured prey was still controversial. For Darwin, natural selection meant that plants wouldn’t have such remarkable adaptations for capturing insects unless there was a good reason for needing them. The final proof that carnivorous plants actually grew better when provided with prey was only later provided by experiments carried out by his son Francis.

 Carnivorous – or not? Nearly everyone is fascinated by carnivorous plants, so in this respect Darwin wasn’t at all unusual. But he had his own reason for studying them in detail, and it’s exactly the same one I referred to earlier when talking about climbing plants. Just as climbing is evidently a gradual development and amplification of behaviour that’s more 104

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Sundew (Drosera rotundifolia) was the subject of much of Darwin’s book on insectivorous plants.

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or less universal in plants, so carnivory clearly starts, at least in its simplest forms, with equipment possessed by most plants. For example, glandular hairs that secrete the sort of mucilage or other compounds needed to trap animals are practically universal among flowering plants, and may often trap and kill small insects, if only by accident. Thus although the more specialised kinds of carnivores may have evolved all kinds of elaborate traps, and sometimes the power of rapid movement, it’s clear that sticky ‘flypaper leaves’ are the first stage in the evolution of these more elaborate forms. Darwin recognised this: Any ordinary plant having viscid glands, which occasionally caught insects, might thus be converted under favourable circumstances into a species capable of true digestion. It ceases, therefore, to be any great mystery how several genera of plants, in no way closely related together, have independently acquired this same power. As there exist several plants the glands of which cannot, as far as is known, digest animal matter, yet can absorb salts of ammonia and animal fluids, it is probable that this latter power forms the first stage towards that of digestion.

Because carnivory evidently evolved in stages, the answer to the question ‘how many carnivorous plants are there?’ is not at all obvious. If we take a fairly strict definition of carnivory, counting only species that have specialised adaptations to attract, capture and digest 106

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animal prey, we’re talking about roughly 1,000 species. But many plants may not have the full set of adaptations, and yet still be carnivorous in a more limited sense.They may, for example, not necessarily secrete their own digestive enzymes, but rely on ‘borrowing’ them from bacteria, fungi or even other animals that eat trapped prey, with the plant absorbing nutrients subsequently released from their faeces. Thus very many more than the thousand or so unambiguous carnivores have some but not all of the carnivorous adaptations and may also be carnivores, even if only in a small way. A nice example of such ‘protocarnivory’ is found in two species of South African subshrubs, Roridula dentata and Roridula gorgonias. Roridula resembles sundews in having leaves covered in sticky glandular hairs that trap insects. Darwin thought Roridula was closely related to sundew (although it isn’t), but he had the benefit only of a dried specimen and never saw the living plant (it gets only one page in his book). In fact Roridula lacks either digestive enzymes or the specialised absorptive glands that allow ‘proper’ carnivorous plants to take up nutrients from dissolved prey. So is it carnivorous at all? Well, yes it is, but in a curiously roundabout way. Two species of bugs (Hemiptera), Pameridea roridulae and Pameridea marthothii, live their entire lives on Roridula, and are never found anywhere else. Like the clown fish that live among the tentacles of sea 107

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Roridula gorgonias, the South African flypaper plant, has unusually sticky, persistent glue. Note the spider lower right, plus assorted prey.

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anemones, they manage to avoid being trapped. Careful investigation has shown that Pameridea eats the prey trapped by Roridula, while the plant benefits from nutrients in the bugs’ faeces. So, exactly like clown fish and anemones, this is a mutualistic relationship. But as in most mutualisms, there’s nothing to stop one partner trying to get more than its fair share. Pameridea also sucks the sap from Roridula, so the plant is not happy if there are too many bugs. Fortunately, the arrangement is policed by a spider, Synaema marlothi, which feeds on both trapped prey and on Pameridea, thus helping to stabilise the symbiotic triangle. Which makes Roridula remarkable enough. But the glue that the plant uses to trap its prey turns out to be even more extraordinary. The suspicion that Roridula glue might be a bit special came from the observation that it seems able to capture surprisingly large insects, so that it’s called vliegebos (fly bush) by South African farmers, who hang its branches in their houses as flypaper. Research quickly revealed that unlike the sticky aqueous mucilage of other flypaper carnivores (sundews and others), Roridula mucilage is a water-insoluble mixture of triterpenoids and acylglycerides: in other words, a resin. What’s more, it appears to be more or less indestructible; the sticky drops remain intact and adhesive on leaves stored dead and dry for five years at least, and even on leaves stored in the preservative formalin. 109

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You can see why Roridula might want desiccationresistant mucilage in the dry summers of its native South African fynbos. But they also experience wet winters, so what happens then? Cue more experiments, which show that the mucilage is waterproof, and works just as well underwater as it does in the dry. The suspicion is that the sticky insect-trapping mucilages of flypaper carnivores can go one of two ways: either the ‘cheap and cheerful’ (but easily replaced) route, or the expensive, waterproof and desiccation-resistant route. Sundews, whose sticky mucilage is 96 per cent water, have gone down the cheap route, while Roridula has gone for the armour-plated option. It’s almost certainly this choice that has compelled Roridula to sub-contract the digestion of its prey to a pair of bugs; the enzymes used by sundews to digest their prey operate in aqueous solution, and a waterproof resin is no use as a digestive medium. Roridula glue is the strongest glue of any sticky plant carnivore. So, the obvious next question is: how do the specialist bugs that live on Roridula avoid becoming stuck? Observations reveal that they make no effort to avoid or remove the glue – they just don’t stick to it. The chemistry of the bug’s cuticle, along with electronmicroscope observations, suggest the answer is a thick layer of grease. The outer layer of grease sticks to the plant resin, but sloughs off as the bug moves about, 110

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preventing the bug itself from becoming stuck. Such greasy layers are not unusual in insects generally, but in most insects they are not thick or continuous enough to protect against Roridula glue. Given that it took years of careful work to figure out what is happening in Roridula, it’s perhaps no surprise that botanists still aren’t always sure as to the purpose of plant glues. For example, the extremely sticky fruits of the New Zealand parapara or bird-catcher tree (Pisonia brunoniana) have frequently been observed to hopelessly ensnare small birds. Since parapara grows on shallow, poor soils, it’s tempting to suggest that the nutrients from dead birds have proved useful, leading to the selection of this unusual trait – in other words, that the plant has evolved to be vicariously carnivorous. But when ecologist Alan Burger investigated, he found that any benefit to the plant’s seedlings was outweighed by damage caused by scavenging crabs that were attracted to the decomposing birds. In fact the extremely sticky seeds probably evolved as a dispersal adaptation, and the mortality of some potential dispersers is just an unfortunate example of collateral damage. Sometimes there’s a clearer gradation of carnivory.The leaf rosettes of many tropical NewWorld bromeliads form rainwater-filled ‘tanks’. Especially in epiphytic species (the majority), water storage is apparently their main function, but the tanks often contain whole ecosystems 111

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of animals, and are important breeding sites for treedwelling frogs. All kinds of detritus, including dead insects, ends up in the tanks, and the plants can absorb the nutrients released by decay and from faeces. But at least one (terrestrial) species has ultraviolet-reflecting scales that attract insects, and digestive enzymes, in other words the full set of carnivorous adaptations.

The New Zealand parapara or bird-catcher tree (Pisonia brunoniana) occasionally catches birds, apparently only by accident Here a trapped Japanese white-eye (Zosterops japonicus) is rescued.

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 Evolution of carnivory Working out the family relationships of carnivorous plants can be highly problematic. One reason is that when plants (or animals) adopt an unusual habitat or lifestyle, the drastic changes to their appearance tend to obscure their normal relationships. There are relatively few ways of being a successful carnivore, so ‘convergent evolution’, where unrelated plants have come to look rather similar, is a particular problem. We now know that true plant carnivory seems to have arisen quite independently at least six times; we can only say ‘at least’ because we can look only at those that have left us some living descendants. Among these surviving species, there is a fairly clear ‘carnivorous habitat’, which can be summed up as ‘lots of light, plenty of water, but not many nutrients’. Nutrients are crucial because only if nutrients such as nitrogen and phosphorous are in really short supply does obtaining them from animal prey seem to pay dividends. Most plants have little difficulty in getting the mineral nutrients they need from soil, in the conventional way. The trap itself is often water-filled, or relies on sticky mucilage; in either case, plenty of available water is an advantage. Waterlogging may also contribute to the nutrient shortage, by inhibiting the release of minerals from decomposing organic matter.

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Not every species conforms to this classic stereotype, but the most familiar temperate carnivorous plants, such as sundews, Venus fly-trap and Sarracenia (the North American pitcher plants), are all plants of open, acid bogs. In short, carnivorous plants live where nutrient shortage makes life difficult, and supplementing the supply by eating animals can make things just a little bit better. But plant carnivory can hardly be described as a runaway success, and although there are many species, they are rarely among the commonest species, even in the most favourable habitats. John Wyndham’s triffids notwithstanding, carnivorous plants seem to have shown no great desire, and still less much ability, to take over the world. For carnivores, good light is useful because traps are nearly always modified leaves, which means carnivorous plants always have to compromise to some extent on photosynthesis. In The power of movement in plants, Darwin was delighted to discover that carnivorous plants broke the rules when it came to responding to light, seeing this as a powerful example of natural selection leading to a somewhat unexpected result: Heliotropism prevails so extensively among the higher plants, that there are extremely few, of which some part, either the stem, flower-peduncle, petiole, or leaf, does not bend towards a lateral light. Drosera rotundifolia is one of the few plants the leaves of which exhibit no 114

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trace of heliotropism. Nor could we see any in Dionaea [Venus fly-trap], though the plants were not so carefully observed. Sir J. Hooker exposed the pitchers of Sarracenia [pitcher plant] for some time to a lateral light, but they did not bend towards it. We can understand the reason why these insectivorous plants should not be heliotropic, as they do not live chiefly by decomposing carbonic acid [i.e. photosynthesis]; and it is much more important to them that their leaves should occupy the best position for capturing insects, than that they should be fully exposed to the light.

 Mechanisms and relationships Carnivorous plants with sticky traps (‘flypaper leaves’) are by far the most numerous kind, and it’s easy to see why – they require the smallest changes from the sort of equipment that most plants have already. Most often sticky hairs are involved (as in sundews), and, as we’ve already seen, Darwin thought Roridula was related to sundews since both have the same kind of sticky tentacles. Darwin put all the plants with such sticky tentacles in the sundew family, but our modern ability to look directly at evolutionary relationships (phylogeny) via DNA has revealed that some of them are not in fact close relatives. Another plant that Darwin thought was a kind of sundew is Byblis, which like Roridula he only ever saw 115

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as a dried specimen (Hooker sent him examples of both from the Kew herbarium). I’ve been fortunate enough to see Byblis on a trip to Australia, and I have to say it looks a lot like a sundew. Unfortunately, Darwin never saw Byblis when he visited Australia; in fact despite being fascinated by carnivorous plants (in which southwest Australia is extraordinarily rich), he was famously unimpressed by that part of the world. As he wrote in the Beagle Diary: The Beagle sailed from Tasmania, and, on the 6th of the ensuing month, reached King George’s Sound, situated near the S.W. corner of Australia. We staid there eight days & I do not remember since leaving England having passed a more dull, uninteresting time ... The general bright green colour of the brushwood & other plants viewed from a distance seems to bespeak fertility; a single walk will however quite dispel such an illusion; & if he thinks like me, he will never wish to take another walk again in so uninviting a country.

And finally, in case you hadn’t already taken the hint: Since leaving England I do not think we have visited any one place so very dull & uninteresting as K. George’s Sound. Farewell Australia, you are a rising infant & doubtless some day will reign a great princess in the South; but you are too great & ambitious for affection, yet not great enough for respect; I leave your shores without sorrow or regret. 116

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Pitcher plants and the Venus fly-trap offer further proof that plant carnivory usually started out with flypaper, which then led on to the development of more specialised traps. However dissimilar they may now appear, both the Venus fly-trap and pitcher plants in the tropical genus Nepenthes are quite closely related to sundews (as is yet another flypaper genus, Drosophyllum), and both therefore seem to have evolved from a flypaper-like ancestor. Presumably, once trapping

Nepenthes distillatoria from Joseph Paxton’s Magazine of Botany of 1838. The species, described as a ‘miraculous distilling plant’, was one of the earliest tropical pitcher plants known to European botanists in the seventeenth century.

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and digesting of prey has evolved in the first place, that makes it much more likely that further modifications to improve its function will evolve. In much the same way, the pitcher plants in the North American Sarraceniaceae (chiefly Sarracenia, but also Darlingtonia and Heliamphora) are related to Roridula. Nepenthes and Sarracenia are a famous example of convergent evolution, demonstrating that if natural selection sets out to turn a leaf into a water-filled trap, whatever kind of leaf you start out with, you will always end up with something that looks about the same.

 Cephalotus and convergent evolution Final proof that there’s really only one way to make a pitcher trap from a leaf is Cephalotus follicularis, the Albany pitcher plant, way out on its own, geographically and taxonomically, in southwest Australia. Cephalotus is not closely related to any other carnivorous plants and seems to be unique in being the only plant with an ‘advanced’ type of trap that lacks a flypaper relative. I’m sorry to say that on my only visit to southwest Australia, I missed Cephalotus, and so did Darwin. In fact although Cephalotus was described in 1806, Darwin makes no mention of it in his book. Which isn’t surprising; if he had decided not to say much about the wellknown Sarracenia and Nepenthes, there was certainly no point saying anything about the much more obscure 118

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Cephalotus follicularis, the Albany pitcher plant, is unrelated to other pitcher plants, and is a classic example of convergent evolution.

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Cephalotus. Darwin was certainly aware of Cephalotus, and rather hoped – as with the other pitcher plants – that Hooker would be able to work on it. But Hooker had even less luck with Cephalotus than he did with the other two, writing at one point to Darwin: ‘As to Cephalotus it is a beast – it will not kill or eat, – & I am in despair about it’. Cephalotus is certainly odd, lying in a branch of the flowering plant family tree with no other carnivores. But that makes it a perfect opportunity to study convergent evolution. On one level, this convergent evolution is completely obvious; even to the most botanically challenged observer, Nepenthes, Sarracenia and Cephalotus look very similar. But is this similarity more than skin-deep? It turns out that it is. We know this because recently an international team sequenced the entire Cephalotus genome, and found that key genes associated with insect attraction, capture, and digestion are basically the same as in Nepenthes and even in the Venus fly-trap, despite these plants evolving carnivory quite independently from Cephalotus. These plants also share proteins with the same apparently random aminoacid substitutions, even though these don’t seem to actually do anything. Are they important for carnivory? They must be, but no-one knows why. Natural selection never invents anything new if some existing structure or behaviour can be modified to do 120

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the job. This principle obviously applies to pitcher traps themselves, which are always modified leaves, but it also applies to the underlying, invisible biology. The same ancestral genes, linked to defence against pathogens or herbivores, seem to have been co-opted in the service of carnivory in a wide range of carnivorous plants. Sometimes it’s very clear how this transformation came about. For example, fungi make their cell walls from a sugar polymer called chitin, so plants typically defend themselves by making enzymes that break down chitin. But insect exoskeletons are made of chitin too, so the same enzyme is pre-adapted to digest captured insects.

 From flypaper to snap-trap Like everyone else, Darwin was fascinated by Dionaea muscipula: ‘This plant, commonly called Venus fly-trap, from the rapidity and force of its movements, is one of the most wonderful in the world.’ Darwin appreciated that the Venus fly-trap is closely related to sundews, something that modern molecular methods have confirmed. He also saw how it could have been derived by gradual modification of a sundew-like ancestor: The parent form of Dionaea and Aldrovanda seems to have been closely allied to Drosera, and to have had rounded leaves, supported on distinct footstalks, and furnished with tentacles all round the circumference, 121

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Venus fly-trap – Dionaea muscipula – is the iconic insectivorous plant. This illustration is by William Curtis (1746–99).

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with other tentacles and sessile glands on the upper surface. I think so because the marginal spikes of Dionaea apparently represent the extreme marginal tentacles of Drosera, the six (sometimes eight) sensitive filaments on the upper surface, as well as the more numerous ones in Aldrovanda, representing the central tentacles of Drosera, with their glands aborted, but their sensitiveness retained.

It’s therefore a great pity that Darwin was unaware of the remarkable abilities of the Australian sundew Drosera glanduligera. This is a relatively common species, but its unusual behaviour was observed only in 1974, and not published until the mid-1990s. Around the edge of its leaves, this sundew has longer, non-sticky tentacles. These tentacles are touch-sensitive and when touched by a passing insect, they rapidly bend inwards, flipping the insect into the central, sticky part of the trap. The researchers who investigated the plant called them ‘catapult tentacles’. This movement takes less than one-tenth of a second – around the same speed as a Venus fly-trap. The mechanism appears to be rapid water movement between cells in the hinge zone at the base of the tentacle, in other words the tentacle itself doesn’t bend, but acts as a lever. The rapid movement fractures the cells in the hinge zone, so the catapult can be fired only once. But this species is a short-lived annual that grows 123

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fast and develops new leaves in only three to four days, so presumably there’s been no great pressure to develop a re-usable system. It’s very tempting to see this supercharged sundew as a ‘missing link’, showing us how a sundew might have taken the first step towards the evolution of a fully fledged snap-trap. It’s easy to imagine how the catapult tentacles, first arising as a way of flipping prey into the sticky trap, might in time have become so effective that the glue was no longer required.

Drosera glanduligera, a sundew with outer ‘snap tentacles’ that catapult prey into the central sticky tentacles. A view of the whole plant [A], close-up of a single leaf showing glue tentacles and snap tentacles [B], and a trap with captured fruit fly [C].

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How the Venus fly-trap evolved seems fairly clear, but another question that bothered Darwin was why it had ever evolved at all.With around 180 species, and present on every continent except Antarctica, Drosera (sundew) is by any measure an extremely successful genus, so why did one of its ancestors evolve into the very different Venus fly-trap? Darwin speculated that the selective pressure was to catch larger insects; his own observations suggested that sundews tended to capture small flying insects, but what did the Venus fly-trap catch? An American correspondent sent him fourteen leaves with prey enclosed: Four of these had caught rather small insects, viz. three of them ants, and the fourth a rather small fly, but the other ten had all caught large insects, namely, five elaters, two chrysomelas, a curculio, a thick and broad spider, and a scolopendra. Out of these ten insects, no less than eight were beetles, and out of the whole fourteen there was only one, viz. a dipterous insect, which could readily take flight. Drosera, on the other hand, lives chiefly on insects which are good flyers, especially Diptera, caught by the aid of its viscid secretion. But what most concerns us is the size of the ten larger insects. Their average length from head to tail was .256 of an inch, the lobes of the leaves being on an average .53 of an inch in length, so that the insects were very nearly half as long 125

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as the leaves within which they were enclosed. Only a few of these leaves, therefore, had wasted their powers by capturing small prey, though it is probable that many small insects had crawled over them and been caught, but had then escaped through the bars.

Modern opinion is that Darwin’s conjecture – that selection would favour the evolution of a trap with interlocking marginal teeth that would release small prey, but retain larger, more rewarding prey – is correct. On the other hand, the complex changes required to evolve a snap-trap, together with the existence of (perhaps) better, more fool-proof ways of capturing larger insects, such as pitcher traps, perhaps help to explain why anything like the Venus fly-trap seems to have evolved only once.

 Aldrovanda You may have noticed an unfamiliar name cropping up among the Darwin quotes in this chapter: Aldrovanda. What is Aldrovanda? A sundew ancestor may have evolved a snap-trap only once, but that event left us with two descendants: one, the Venus fly-trap, that literally everyone has heard of, and one that almost no-one has heard of: Aldrovanda vesiculosa, the waterwheel plant. Darwin described it as ‘a miniature aquatic Dionaea’, and devoted a full (albeit short) chapter to it. Remarkably, Aldrovanda is the most widely distributed carnivorous plant in the world, native to almost everywhere except 126

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Aldrovanda vesiculosa, the waterwheel plant, is a kind of underwater Venus fly-trap (as illustrated in Darwin's book on insectivorous plants).

the Americas. It’s also – I think – an extremely graceful plant, a rootless, free-floating aquatic with whorls of leaves, each terminating in a trap very much like those of the Venus fly-trap. From the right angle, it is indeed very waterwheel-like. Like the Venus fly-trap, Aldrovanda has the full set of carnivorous adaptations, including secretion of digestive enzymes; Darwin observed of a trapped beetle, ‘All the softer tissues of this beetle were completely dissolved, 127

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and its chitinous integuments were as clean as if they had been boiled in caustic potash’, although he noted that the plant normally caught small aquatic crustaceans and insect larvae.

 From butterworts to bladderworts Meanwhile, in another part of the taxonomic forest altogether, a further group of plants had also invented carnivory, beginning as usual with fly-paper and ending up with something quite unique. These are the plants in the Lentibulariaceae, the butterwort and bladderwort family; the whole family is carnivorous. Butterworts (Pinguicula) have sticky leaves, but so do many plants, and although many people had noticed that insects (along with other bits of detritus) were found stuck to the leaves, no-one knew if butterwort was carnivorous or not. As Darwin noted, ‘I was led to investigate the habits of this plant by being told by Mr. W. Marshall that on the mountains of Cumberland many insects adhere to the leaves’. Darwin confirmed this by his own observations, and then conducted numerous careful experiments, which demonstrated clearly that butterworts digest their prey and absorb the nutrients released: We thus see that numerous insects and other objects are caught by the viscid leaves; but we have no right 128

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to infer from this fact that the habit is beneficial to the plant, any more than in the before given case of the Mirabilis, or of the horse-chestnut. But it will presently be seen that dead insects and other nitrogenous bodies excite the glands to increased secretion; and that the secretion then becomes acid and has the power of digesting animal substances, such as albumen, fibrin, &c. Moreover, the dissolved nitrogenous matter is absorbed by the glands, as shown by their limpid contents being aggregated into slowly moving granular masses of protoplasm. The same results follow when insects are naturally captured, and as the plant lives in poor soil and has small roots, there can be no doubt that it profits by its power of digesting and absorbing matter from the prey which it habitually captures in such large numbers.

Butterworts have other interesting properties, of which Darwin was unaware. For example, butterwort leaves produce a bactericide that prevents insects from rotting while being digested. This property was known to traditional medicine, which used butterwort leaves to heal sores and clean wounds in both humans and animals. Leaves of butterwort – and also sundew – have also a traditional use in Scandinavia for curdling milk to form a buttermilk-like fermented milk product called filmjölk (Sweden) and tjukkmjølk (Norway). Presumably the protein-degrading enzymes produced by the leaves of these plants are acting as a kind of vegetable rennet. 129

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Butterwort – Pinguicula vulgaris – from Dr Otto Wilhelm Thomé’s Flora von Deutschland, Österreich und der Schweiz (1885).

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Butterworts are small plants of wet, open places. In contrast, the temperate species of bladderworts are usually rootless, floating aquatics and look quite different until they flower, when their close relationship to butterworts becomes obvious. Indeed, this was one of the reasons why Darwin first became interested in them: I was led to investigate the habits and structure of the species of this genus partly from their belonging to the same natural family as Pinguicula, but more especially by Mr. Holland’s statement, that ‘water insects are often found imprisoned in the bladders’, which he suspects ‘are destined for the plant to feed on’.

The 200 or so species of bladderwort are extremely widely distributed, and as well as the familiar aquatics, there are terrestrial, epiphytic and even climbing species. Darwin devoted most attention to the aquatics, but also looked at some terrestrial species. In all cases, as he noted, ‘The bladders offer the chief point of interest’. The bladders have little trapdoors and catch small aquatic animals, often in large numbers. Dismissing the idea that the bladders act as floats, he says: ‘The real use of the bladders is to capture small aquatic animals, and this they do on a large scale.’ Darwin failed to demonstrate the ability of bladderworts to digest their prey, but wasn’t sure that they couldn’t, noting ‘the suspicion that the bladders secrete some ferment hastening the process of decay’. But in any 131

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case, he was sure that ‘Whether or not the decay of the imprisoned animals is in any way hastened, it is certain that matter is absorbed from them by the quadrifid and bifid processes’. And this, coupled with some kind of trapping ability, is perhaps the most important part of carnivory. Plenty of carnivorous plants don’t bother with digestion, being more than happy to let animals or microbes deal with this.We saw this in Roridula, and – as we shall see – it’s common in pitcher plants. At this point, however, Darwin’s normally acute powers of observation and deduction let him down. How, he wondered, do so many animals end up in the bladders? As he ponders this question, you can almost feel his puzzlement through the page: ‘It is difficult to conjecture what can attract so many creatures, animaland vegetable-feeding crustaceans, worms, tardigrades, and various larvae, to enter the bladders’. And: ‘Perhaps small aquatic animals habitually try to enter every small crevice, like that between the valve and collar, in search of food or protection.’ Yet when you read his account, it’s evident that he came very close to the truth; indeed, he made the observations that might have allowed him to deduce what was going on, but failed to appreciate their significance: On three occasions minute particles of blue glass (so as to be easily distinguished) were placed on valves whilst under water; and on trying gently to move them with 132

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a needle, they disappeared so suddenly that, not seeing what had happened, I thought that I had flirted them off; but on examining the bladders, they were found safely enclosed. The same thing occurred to my son, who placed little cubes of green box-wood (about 1/60 of an inch [0.423 mm]) on some valves; and thrice in the act of placing them on, or whilst gently moving them to another spot, the valve suddenly opened and they were engulfed.

Bladderworts (Utricularia species) are carnivorous plants that build special organs (‘bladders’) to trap small creatures. Here we see a shoot of U. vulgaris, showing the numerous underwater bladders.

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In fairness to Darwin, the bladderworts’ traps operation is far too fast to be followed with the naked eye. Only with modern high-speed cameras, capable of up to 15,000 frames per second, has it been possible to study exactly how they work. In its ‘relaxed’ state, the trap is a slightly flattened cylinder, with two opposing, convex walls. The plant sets the trap by pumping water out of the bladder until the walls are sucked inwards, eventually becoming concave. At this stage, the trapdoor at one end of the cylinder is a shallow dome with its convex face outward, so it resists the pressure of the water outside the trap, rather like a stone arch supports the weight above it. At the base of the trapdoor are long trigger hairs, and when one of these is touched by a passing crustacean, the trapdoor suddenly opens inward, the stored elastic energy in the bladder is rapidly converted into kinetic energy, and both water and prey are sucked inside the bladder. It was this that Darwin observed, although it was far too fast for him to make out what was happening. How the trigger works is still something of a mystery. We know triggering causes buckling of the trapdoor, which rapidly reverses its curvature from convex to concave, in which state it can no longer resist the external pressure, so it swings open. But we don’t know whether the trigger hair acts as a simple mechanical 134

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lever, or whether it activates some kind of electrical or chemical switch. The whole trapping sequence lasts approximately three milliseconds, with a suction phase of only half a millisecond.This is by far the fastest trapping movement of any carnivorous plant, and in fact one of the

Close-up of a Utricularia bladder. The trap is triggered when prey touch the long trigger-hairs around the entrance.

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fastest movements known in the plant kingdom. The maximum velocity of the water sucked into the trap is 1.5 m s-1, giving a maximum fluid acceleration of 600g. What this means, if you’re a water flea that happens to touch a trigger hair, is that what happens next is far too fast to avoid, or even to notice; one moment you’re paddling along, minding your own business, the next you’re inside a trap, with no idea how you got there. Finally, the prey is dissolved by digestive enzymes secreted by glands, the nutrients are absorbed by the plant, and the trap is ready to go again. It’s an ingenious process – and one that can be of use to humans, too. Recently, in Portugal, I met a designer who builds swimming ponds in which the water is cleaned by natural processes. To help to control the larvae of mosquitoes and other aquatic insects, he adds Utricularia to the water. Apparently it works, and, for the botanically inclined swimmer, it adds a new dimension to the whole experience. And, before taking leave of bladderworts, I have to mention Utricularia humboldtii, whose only known habitat is the water tanks of Brocchinia, the only unambiguously carnivorous bromeliad. How weird is that? But butterworts and bladderworts do not exhaust the Lentibulariaceae. There is a third genus, Genlisea, rootless like the bladderworts, some species aquatic, some terrestrial, but entirely tropical. Darwin devoted 136

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the final few pages of his Utricularia chapter, indeed the last section of his book on insectivorous plants, to Genlisea, and made remarkable observations, despite having only preserved specimens to work on (sent, as usual, from Kew by Hooker). Genlisea has ordinary leaves, but below ground (or underwater) it has leaves modified into the most peculiar traps.The solid, thin lower part of the leaf opens into a bulb and then contracts into a tube that divides at the end into two spirally contorted arms, hence

Genlisea violaceaXQHDUWKHGWRVKRZVXEWHUUDQHDQ×FRUNVFUHZWUDSVØb

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the common name ‘corkscrew plants’. The arms have narrow openings and small animals, such as nematodes, protozoa, rotifers, worms, crustaceans and mites, enter and cannot escape owing to numerous backwardly directed hairs. Eventually they end up in the bulb where they are digested and the nutrients absorbed.The whole thing resembles a traditional eel-trap, as Darwin noted: ‘animals are captured by Genlisea … by a contrivance resembling an eel-trap, though more complex.’ Darwin didn’t know what persuaded prey to enter the trap, but the latest research has shown that the plants secretes chemicals that attract prey into the trap. While it’s very possibly unrelated to carnivory, indeed almost certainly, it’s still worth relating one last surprising thing about the Lentibulariaceae. For reasons that aren’t always clear, but which probably merit a whole book of their own, plant genomes vary enormously in size. At the small end of the scale, the record holder was long thought to be the plant geneticist’s favourite Arabidopsis thaliana, but it turns out that two species of Genlisea have genomes less than half the size. The Utricularia genome is tiny too, but Genlisea holds the record – its genome is only the same size as that of a bacterium. The largest known genome, of Paris japonica (a relative of the European woodlander herb Paris, Paris quadrifolia) is 2000 times larger; the DNA from a single Paris cell stretched out end-to-end would be 91 m long. 138

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 Pitcher plants I have noted already one or two things that Darwin seems to have chosen deliberately not to investigate. But here is the real elephant in the room, as far as carnivorous plants are concerned. There are two great groups of pitcher plants, the temperate Sarraceniaceae and the tropical Nepenthaceae, and Darwin has very little to say about either. True, he makes passing reference to both, in the context of the ability (or lack of it) to digest captured prey. But that’s it – he doesn’t even tell us why he leaves them out of an otherwise comprehensive book. This omission is all the more remarkable when you consider that Darwin was writing at the height of the Victorian obsession with the Gothic, with the public devouring travellers’ tales of wholly imaginary tropical man-eating trees (Madagascar was a favourite location). And Southeast Asian Nepenthes, an inhabitant of the classic steamy jungle, is the closest fit to these imaginary plants. Even the largest, such as the recently discovered Nepenthes attenboroughii, are admittedly not man-eaters, but they are big enough to catch the odd rat or lizard. A cultivated specimen in Somerset famously caught (and presumably ate) a great tit, although records of birds being caught are more or less unknown in the wild. Of course, many Nepenthes are quite large, they need proper hothouse conditions, and the species aren’t all that easy to grow. In fact Darwin’s correspondence 139

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with Hooker shows that he hoped Hooker would be able to experiment on them on his behalf. It looks like Hooker, helped by the Assistant Director of Kew, William Thiselton-Dyer, did actually make some progress with Nepenthes, but not enough to persuade

Nepenthes veitchii from Borneo, an epiphytic member of the large genus of tropical pitcher plants. The brightly coloured rim of the trap attracts insects.

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Darwin to include them in his book. In the end he simply notes that fluid from Nepenthes pitchers certainly has the power of digestion, as Hooker had been able to demonstrate. Sarracenia, by contrast, are hardy herbaceous plants, not all that difficult to grow if you can give them the right sort of acid, boggy conditions. Sarracenia purpurea is well established in several locations in Britain and Ireland. Perhaps Darwin simply decided that if he couldn’t do the pitcher plants properly, he wouldn’t do them at all. He may also have been discouraged by Hooker’s report that he couldn’t get the Sarracenia species he was working on to secrete anything at all. I have a sneaking suspicion that Darwin had a soft spot for the more ‘active’ carnivorous plants. Insectivorous Plants has eighteen chapters, and twelve of them are about sundews. Two others are about the Venus fly-trap and Aldrovanda, both with snap-traps, and two more are about bladderworts, also with active traps – although Darwin failed to realise that. Darwin was never happier than when feeding his sundews with all manner of stuff, to see what would make them react and what wouldn’t: Small bits of raw meat (which acts more energetically than any other substance), of paper, dried moss, and of the quill of a pen were placed on several leaves, and they were all embraced equally well in about 2 hrs. On other occasions the above-named substances, or more 141

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commonly particles of glass, coal-cinder (taken from the fire), stone, gold-leaf, dried grass, cork, blotting-paper, cotton-wool, and hair rolled up into little balls, were used, and these substances, though they were sometimes well embraced, often caused no movement whatever in the outer tentacles, or an extremely slight and slow movement. Yet these same leaves were proved to be in an active condition, as they were excited to move by substances yielding soluble nitrogenous matter, such as bits of raw or roast meat, the yolk or white of boiled eggs, fragments of insects of all orders, spiders, &c.

Darwin wrote in a letter to his geologist friend Charles Lyell, at the time when he was most deeply involved in his sundew experiments, ‘at this moment I care more about Drosera than the origin of all the species in the world’. Elsewhere he refers more than once to ‘my beloved Drosera’, and writes ‘I have been infinitely amused by working at Drosera’, and ‘I will stick up for Drosera to the day of my death’. Darwin’s insectivorous plant book could almost as accurately have been called his sundew book. Indeed he refers to it himself, in a letter to American botanist Asa Gray, as ‘my book on Drosera & Co.’, and he may have thought, or at least feared, that pitcher plants were just not very exciting in comparison. The one thing Darwin thought he knew about pitcher plants, on the evidence of his book, is that Nepenthes possessed the ability to 142

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secret digestive enzymes, and that Sarracenia did not, but in both cases he was relying on the observations of others, and they were not entirely correct – at any rate about Sarracenia. In fact, although Darwin was fairly sure that Sarracenia did not secrete digestive enzymes, he decided to hedge his bets, noting that ‘the fact can hardly be considered as yet fully proved’. We now know that Sarracenia can secrete digestive enzymes, but not in large amounts, and that it is mostly happy to let bacteria, algae, protozoa and insect larvae do the job instead. In reality the ability to secrete digestive enzymes is hugely variable across the pitcher plants. At one extreme most species of the Sarracenia relative Heliamphora don’t produce enzymes, and in fact don’t secrete any liquid into the pitchers at all, relying on rainwater, and as a result the lid that normally covers the pitchers of most species is much reduced. The ability to secrete digestive enzymes is generally well developed in Nepenthes, but even here, many species have preferred to evolve mutualistic relationships with other species. Some of these have involved largely giving up carnivory in favour of other sources of nutrients; for example, not only do the pitchers of many species look like toilets, some of them actually are; Nepenthes lowii pitchers are used as a toilet by the tree shrew Tupaia montana. The plant produces large amounts of nectar to attract the shrews and then absorbs nutrients from their 143

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faeces; over half, and sometimes all, of the nitrogen in the leaves of the plant comes from tree shrew faeces. In a variation on the same theme, Nepenthes rajah is also used as a toilet by the tree shrew Tupaia montana during the day, and at night by the nocturnal rat Rattus baluensis. It’s the nectar-secreting lid that attracts both mammals, which positions the animals perfectly over the pitcher to collect their faeces. And since tree shrews are dichromatic – having only two types of cone cell in the retina, sensitive to blue and green light – the pitcher lid brightly reflects both blue and green, perfectly tuned to the shrew’s vision.The pitchers also release strong fruity and flowery odours that attract both mammals. This arrangement seems to work well almost all the time, for both the plants and the animals, though researchers who examined forty-two active Nepenthes rajah traps did find the body of a tree shrew in one of them. Nepenthes hemsleyana, from Borneo, has gone one step further. When researchers looked at this species, they were surprised to discover that it is ineffectual in trapping prey; instead its pitchers are unusually large and are used as daytime roosts by the bat Kerivoula hardwickii. The bat is protected from rain and predators, while its faeces provide over a third of the plant’s nitrogen. Further research continues to reveal the extent of the co-evolution between the bat and the plant: its pitchers are large enough to accommodate a bat mother and 144

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Hardwicke’s woolly bat (Kerivoula hardwickii) arriving at a pitcher plant (Nepenthes hemsleyana) to roost, Brunei.

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its baby, while a sharp taper in the shape of the pitcher allows the bat to wedge itself comfortably into the pitcher without having to try to hang on to the slippery sides, and removes the danger of falling into the fluid in the base of the trap. Even more remarkably, recent research has shown that the pitcher of Nepenthes hemsleyana is modified into a special acoustic reflector that makes it easier for the bats to echo-locate, and distinguishes it from closely related species that don’t make good roosts. Darwin would have been delighted by all this evidence of natural selection in action, but one can begin to see why investigating these plants was a bit beyond his normal ‘kitchen-sink science’ modus operandi.

 Housekeeping ants Many plants have a symbiotic association with ants, providing them with living space; in return, the ants often prune encroaching competitors or attack herbivores. Not surprisingly, despite sometimes eating ants and other insects, Nepenthes has developed similar relationships. For example, the Bornean species Nepenthes bicalcarata has swollen, hollow pitcher tendrils that provide nesting space for its ant partner Camponotus schmitzi. Noone knows how, but the ants can run safely across the slippery trapping surfaces of the pitcher without falling in; they also feed on the nectar the pitcher produces to attract prey, and can dive and swim in the pitcher 146

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fluid, where they hunt for prey and retrieve drowned food. Great for the ants, obviously, but for a long time it wasn’t understood what the plant gets out of it. An early suggestion was that the ants break down large prey and thus reduce putrefaction of the pitcher contents. But such putrefaction may be a good thing, since the pitchers readily absorb the ammonia produced. Another suggestion is that the ants do what the ants in such a partnership often do, which is protect the plant from herbivory. And maybe they do, in a small way, though Camponotus doesn’t seem to be particularly aggressive. A third possibility is that the ants attack prey that has fallen into the pitcher and prevent them escaping. But observations show that the pitchers are quite good at this on their own. A clue to what the ants actually do comes from the way the pitchers work. The pitcher rim is formed by smooth, overlapping epidermal cells, which provide no grip for insects attempting to escape from the pitcher. The rim is also highly wettable and is covered by a thin film of water. Insects that step on to this surface ‘aquaplane’ into the pitcher, where they drown and are digested. This works beautifully, but only if the pitcher is clean; if it becomes contaminated by dirt or fungi, it becomes less slippery and doesn’t work so well. Which is where the ants come in. Recent research has found that the ants regularly clean the pitcher rim, 147

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and that this behaviour increases the carnivorous plant’s capture efficiency. Compared to pitchers lacking ants, antcolonised pitchers captured almost 50 per cent more prey. The researchers also found that if they experimentally contaminated pitchers with starch, which completely stopped them working, the ant ‘janitors’ returned them to a perfectly clean state within a week. So effective is this cleaning that ant-free pitchers quite rapidly stop working owing to contamination of the pitcher rim, but ant-colonised pitchers still work as efficiently as newly opened pitchers after sixteen months.

 Slippery or sticky? Nepenthes bicalcarata has an effective and (once understood) perhaps obvious pitfall trap: anything that steps on the smooth, slippery edge is rapidly dumped into the pool of digestive liquid below. But are all pitcher plants like this? A slippery edge is a good tactic against crawling insects; even if they escape from the liquid and crawl up the inside of the pitcher, once they reach the slippery, waxy area, they promptly slide back in again. On the other hand, observations have shown that this kind of trap is relatively ineffective in trapping flying insects; if they escape from the liquid, they can simply fly out. Pitcher plants that specialise on flies seem therefore to have come up with an alternative strategy, which is to have long-chain 148

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‘viscoelastic’ polymers in the liquid. Once insects come into contact with the viscoelastic liquid, they have little chance of escaping; the more they struggle, the more the fluid resists their movements and they rapidly become exhausted and drown. But whether they specialise on ants or flies, the genuinely insectivorous pitcher plants mostly share a suite of adaptations that increase prey capture. These include nectar and flowery odours to attract insects to the traps, and sometimes a bit of chemical warfare on the side. The nectar of Sarracenia flava contains the alkaloid coniine, an insect anaesthetic. Researchers who watched insects visiting the pitchers of Nepenthes madagascariensis saw that insects might spend thirty minutes or more consuming nectar from an individual pitcher. Over this time they became visibly more dizzy and disoriented, before eventually falling into the pitcher. The cause seems to be volatile alkaloids and essential oils; not only did chemical analysis reveal these chemicals, but the researchers themselves found that after working with the pitchers over a few hours they also developed headaches and began to feel dizzy.

 No moving parts? Whether adapted to catch insects or harvest mammal faeces, pitcher plants are all basically pitfall traps. Or at least, nearly all. Darlingtonia californica, a relative of 149

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Darlingtonia californica — the California pitcher plant or cobra lily, owing to the resemblance of the pitcher to a rearing cobra.

Sarracenia, is unique in a number of ways. In the first place, pitcher plants generally contain a mixture of liquid secreted by the plant itself and (inevitably) rainwater. But Darlingtonia regulates the pitcher water level by pumping water up through its roots. It also doesn’t use rainwater, because the top of the pitcher curves over (hence the name, cobra lily) and the entrance faces downwards. 150

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Clearly, nothing can actually fall into the upwardfacing pitcher mouth, but that doesn’t stop it being highly effective. The usual nectar and scent attract insects that find their way into the open mouth. Once there, they are attracted by the light admitted by glassy, translucent windows in the sides of the pitcher, take a step onto the slippery lip of the tube, adorned with downward-pointing hairs, and fall to their digestive doom.The whole thing is far more than the usual pitfall trap, and indeed has much in common with a lobster pot. Weird as Darlingtonia may be, it follows the rule in one important aspect that we can all agree on: pitcher plants have no moving parts. Or do they? Most pitchers have lids, and the lid is normally there to prevent the pitcher filling up with rainwater, but in Nepenthes gracilis (and only in this species), the lower surface of the lid is covered with a slippy wax layer a bit like that on the inner walls of the pitcher.There are other unusual things about this lid. Compared to similar related species, the lower surface also produces lots of nectar, and the whole lid is unusually stiff. What does all this add up to? Well, as the researchers who worked this out put it, ‘the pitcher lid of Nepenthes gracilis resembles a stiff plate articulated with a basal torsional spring’. In simple terms, when the lid is struck from above by raindrops, it rapidly vibrates. Peak lid velocity is nearly 1.5 metres per second, with 151

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Nepenthes gracilis pitcher with ant feeding on nectar secreted by the lid. Raindrops striking the stiff pitcher lid cause it to vibrate, throwing visiting ants into the trap.

a maximum acceleration of almost 300 ms−2. In other words, an order of magnitude faster than the snap-traps of the Venus fly-trap; the only carnivorous traps that move faster are the suction traps of bladderworts. The result is that ants, happily helping themselves to the nectar on the underside of the lid, are violently thrown into the pitcher before they know what hit them. What makes Nepenthes gracilis particularly dangerous, from the ants’ perspective, is the unpredictability of 152

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this behaviour. Normally the trap lid is a perfectly safe source of nectar, but a single raindrop transforms it into a lethal trap, which makes it very hard for the ants to avoid being caught. Darwin could hardly have asked for a better example of how relatively minor evolutionary changes can provide an existing organ with a new and quite unexpected function.

 Triphyophyllum peltatum As we’ve seen, there are carnivorous plants that Darwin chose not to investigate.Then there are those he couldn’t study, because they were unknown at the time. One of these, and one that breaks most of the ‘rules’ of carnivory, is Triphyophyllum peltatum. Triphyophyllum eschews the ‘classic’ open, sunny habitat of most carnivorous plants. A liana confined to the tropical rain forests of Sierra Leone, Liberia and Ivory Coast, it may be seen as an African analogue of the Southeast Asian Nepenthes. Like many lianas, Triphyophyllum is heterophyllous, that is it has different kinds of leaves at different stages of its life cycle. Juvenile leaves look very ordinary: long, narrow and very leaf-like. But just before the peak of the rainy season it grows clusters of very narrow glandular leaves, bearing both stalked and sessile glands. These are very effective insect traps, and Triphyophyllum has the full set of carnivorous adaptations, since they also secrete 153

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digestive enzymes. The stalked glands are the most anatomically elaborate known in the plant kingdom. The insect-trapping leaves are only short-lived, and the plant then graduates to a climbing form that produces yet another kind of leaf, with two grappling hooks on the end of each one. At this point it gives up on the glandular leaves and the mature liana is not carnivorous. So not only does Triphyophyllum grow in a very atypical, shady habitat, it’s only a ‘part-time’ carnivore. And there’s one more Triphyophyllum peltatum – well surprising thing about worth commemorating. this extraordinary plant; it is the source of a number of naphthy-lisoquinoline alkaloids with very promising anti-malarial activity.

 Underground carnivory One of the things we think we’ve known ever since Darwin’s work is that ‘proper’ carnivores, those with the full set of carnivorous adaptations, are found in a small number of well-known plant families, most of which are wholly carnivorous. But Triphyophyllum and its two 154

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sister genera (neither carnivorous) make up a whole new family, the Dioncophyllaceae, which was only described in the 1950s. Even more recent, in a species only described in 2000, is a new example of carnivory in a large and familiar family with no other carnivorous members – as far as we know. This plant turned up in the Campos Rupestres of the Central Brazilian cerrado, an extremely species-rich area of well-lit and low-nutrient rock outcrops and shallow, white sands. It’s the sort of desperately nutrient-poor place that might be expected to support carnivorous plants, and indeed it’s home to several species in the genus Genlisea (a relative of the butterworts and bladderworts we discussed earlier). Research published in 2012 has shown that the small plant Philcoxia has sticky underground leaves that trap and digest nematode worms. It’s the first plant that’s been shown to do this, and it’s in a large family – the Plantaginaceae – in which carnivory is otherwise unknown. So not only does it add another plant family to those known to contain carnivores, it also increases from six to seven the number of occasions on which carnivory appears to have independently evolved. It also confirms, in case it needed any confirming, that there is a lot going on below ground, especially in terms of interactions between plants and other organisms, that we still don’t understand. 155

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CHAPTER

4

Sex and the Single Plant On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing (1862) The effects of cross and self-fertilisation in the vegetable kingdom (1876) The different forms of flowers on plants of the same species (1877)

W

e’ve looked already at three of Darwin’s six botanical books. The remaining three are about sex, or at least about flowers, which in botany amounts to the same thing. These three books are probably best seen as a kind of trilogy, so I’ll look at all three together. 156

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 Orchid fertilisation In the earliest book, on orchid fertilisation, all the usual Darwinian themes are evident. In particular, that all behaviours, organs and structures are slowly and gradually modified by natural selection, often ending up a long way from where they started: It has, I think, been shown that the Orchideæ exhibit an almost endless diversity of beautiful adaptations. When this or that part has been spoken of as adapted for some special purpose, it must not be supposed that it was originally always formed for this sole purpose. The regular course of events seems to be, that a part which originally served for one purpose, becomes adapted by slow changes for widely different purposes.

Also as usual, when Darwin was immersed in his latest project, he became obsessed to the exclusion of almost everything else. In one letter to Joseph Hooker, he wrote: ‘I never was more interested in my life in any subject than this of orchids’, and in another, remarking on the mechanism of pollen transfer in pyramidal orchid: ‘I never saw anything so beautiful.’ As in The Origin, Darwin was at pains to point out, often over and over, that just because something seemed perfectly designed for a particular purpose, that didn’t mean that it had actually been designed: Although an organ may not have been originally formed for some special purpose, if it now serves for 157

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this end, we are justified in saying that it is specially adapted for it. On the same principle, if a man were to make a machine for some special purpose, but were to use old wheels, springs, and pulleys, only slightly altered, the whole machine, with all its parts, might be said to be specially contrived for its present purpose.

The result, in the orchids, was impressive: In my examination of Orchids, hardly any fact has struck me so much as the endless diversities of structure – the prodigality of resources – for gaining the very same end, namely, the fertilisation of one flower by pollen from another plant.

Notice not just fertilisation, but cross-fertilisation; although hardly any effort at all is required to get pollen from one part of a flower to another part of the same flower, it’s much harder to get pollen reliably transported to a different flower of the same species. The main theme of both Darwin’s later flower-books was why all that effort was necessary. But, Darwin noted, the orchids really do seem to have brought more cunning to the process of insect pollination than other kinds of plants: It may naturally be inquired, Why do the Orchideæ exhibit so many perfect contrivances for their fertilisation? From the observations of various botanists and my own, I am sure that many other plants offer analogous adaptations of high perfection; but it seems 158

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that they are really more numerous and perfect with the Orchideæ than with most other plants.

To digress briefly, Darwin would have been even more impressed by orchids’ ‘perfect contrivances’ if he had been aware of deceptive pollination, where orchids exploit insects as pollinators without providing any reward, often by subverting the insects’ sexual impulses for their own purposes. In fact Darwin was aware of

The orchid marsh helleborine (Epipactis palustris) being pollinated by a beetle. The orchid pollinia (pollen masses) can be seen attached to its head.

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reports of orchids that produced no nectar, and even satisfied himself that this was indeed the case in several species. However, he couldn’t bring himself to believe that insects were stupid enough to be fooled by ‘so gigantic an imposture’, and deceptive pollination would not be recognised until the twentieth century. Just asking the question shows Darwin’s thinking at its best. Orchids do indeed display the most jaw-dropping adaptations for pollination, and it’s easy to be sucked into mere admiration for such wondrous botanical sexiness. But Darwin wasn’t just impressed – he wanted to know why. And not only did Darwin ask the question, he knew the answer. In the first place orchid pollen is unusual in being produced in large packets called pollinia, which is necessary because orchids seeds are extremely small, and correspondingly numerous: as the seeds produced by Orchids are so inordinately numerous, we can see that it is necessary that large masses of pollen should be left on the stigma of each flower … This circumstance apparently explains why the grains cohere in packets or large waxy masses, as they do in so many tribes, namely, to prevent waste in the act of transportal.

But putting all your eggs in one basket is not without its risks, and the loss of a pollinium is a disaster. Darwin saw that pollinia had allowed orchids to economise on pollen, 160

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but natural selection had also compelled them to make sure they were transported to exactly the right place: If the Orchideæ had elaborated as much pollen as is produced by other plants, relatively to the number of seeds which they yield, they would have had to produce a most extravagant amount, and this would have caused exhaustion. Such exhaustion is avoided by pollen not being produced in any great superfluity owing to the many special contrivances for its safe transportal from plant to plant, and for placing it securely on the stigma. Thus we can understand why the Orchideæ are more highly endowed in their mechanism for crossfertilisation, than are most other plants.

Modern research has tended to support Darwin’s view of why pollinia evolved in the first place, and also why orchids have particularly ‘perfect contrivances’ for delivering them to their targets. But every adaptation has its price, and although the road taken by orchids has greatly increased the efficiency of pollination, it has also made them far more dependent than most plants on their specialist pollinators.

 Angraecum sesquipedale ‘The Angræcum sesquipedale, of which the large six-rayed flowers, like stars formed of snow-white wax, have excited the admiration of travellers in Madagascar, must not be passed over.’ Indeed it must not, and even though 161

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the story is well known, it will bear one more re-telling. As Darwin noted, in this species: A green, whip-like nectary of astonishing length hangs down beneath the labellum. In several flowers sent me by Mr. Bateman I found the nectaries eleven and a half inches long, with only the lower inch and a half filled with nectar. What can be the use, it may be asked, of a nectary of such disproportionate length?

This was the sort of question Darwin loved. And, after the construction of his new greenhouse at Down House in 1863, he was at last in a position to give tender plants like Angraecum the conditions they needed. As he put it in a letter to Hooker: ‘the new Hothouse is ready & I long to stock it, just like a school-boy.’ This letter was written in February, and although Darwin had already given Hooker a list of plants he hoped to get from Kew, he couldn’t bear to wait until spring; and asks if ‘stove’ (i.e. hothouse) plants would survive the journey from Kew to Down on a cold winter’s day? They would – and only a week later, Darwin writes to thank Hooker for a hothouse-full of plants: ‘The Plants arrived quite safe last night.’ Today, a potted Angraecum is among the many plants in the greenhouse at Down, but as the present head gardener ruefully acknowledges, it isn’t the easiest plant to persuade to flower. After much careful observation and experiment on Angraecum, Darwin concluded that: ‘The pollinia 162

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Darwin’s moth – a drawing by Thomas Wood that accompanied an article on ‘Creation by Law’ by Alfred Russel Wallace.

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would not be withdrawn until some huge moth, with a wonderfully long proboscis, tried to drain the last drop.’ He admitted that ‘This belief of mine has been ridiculed by some entomologists’, but was unmoved; the orchid must be pollinated by something, and he had satisfied himself that he knew exactly what that something must look like. Mendeleev himself, having assembled the periodic table of the elements, was not more certain that he could predict the properties of the hitherto undiscovered ‘missing’ elements. It took more than forty years for the predicted pollinator, the hawkmoth Xanthopan morganii var. praedicta, to be discovered in the forests of Madagascar, and the demonstration of pollination of the orchid by this animal had to wait until 1997. Darwin imagined the orchid’s spur and the moth’s proboscis evolving together in a kind of arms race, with every stage making both the orchid’s reproduction and the moth’s foraging more efficient. An alternative evolutionary model imagines that long tongues in the hawkmoth pollinators were present before the long spurs of the orchids evolved, with longer spurs evolving as the orchids moved on to pollinators with successively longer tongues. We still don’t know which model is correct. Modern opinion tends to favour the second hypothesis, but both models essentially agree with Darwin’s idea that longer spurs 164

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evolved in response to the selective pressure exerted by long-tongued pollinators. One thing’s for sure – there’s an awful lot of interesting orchid-pollinator co-evolution to be discovered in Angraecum and closely-related genera, and we still know hardly any of it. Fewer than twenty of the more than 760 species have been investigated and, although hawkmoths are the commonest pollinators, some species have clearly evolved to be pollinated by birds, and others (very unusually) by crickets.

 Darwin and the gardeners – part 1 Tropical orchids were a Victorian obsession, so it’s not surprising that Darwin’s orchid book was a sensation. A review in the Gardeners’ Chronicle by John Lindley, the world’s foremost authority on orchids at the time, stretched across three issues. Lindley shared none of the entomologists’ scepticism about Darwin’s predicted long-tongued pollinator: The answer is necessarily conjectural in a great degree, but every hypothetical step in his reasoning being shown to be founded on observation of what occurs in analogous forms of orchids, we are compelled to acknowledge that the explanation is in the highest degree probable.

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can be gained from a letter from Joseph Hooker to a correspondent: Darwin still works away at his experiments and his theory, and startles us by the surprising discoveries he now makes in botany; his work on the fertilisation of orchids is quite unique – there is nothing in the whole

Joseph Hooker, Darwin’s closest friend and for twenty years Director of the Royal Botanic Gardens, Kew.

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range of botanical literature to compare with it, and this, with his other works … raise him without doubt to the position of the first naturalist in Europe, indeed I question if he will not be regarded as great as any that ever lived; his powers of observation, memory and judgement seem prodigious, his industry indefatigable and his sagacity in planning experiments, fertility of resources and care in conducting them are unrivalled.

 Cross-fertilisation and natural selection There is weighty and abundant evidence that the flowers of most kinds of plants are constructed so as to be occasionally or habitually cross-fertilised by pollen from another flower, produced either by the same plant, or generally, as we shall hereafter see reason to believe, by a distinct plant.

Thus begins Darwin’s 1876 book on the subject of cross-fertilisation. He then admits that adaptations for cross-fertilisation in plants had interested him for the past thirty-seven years. But why this abiding interest? As Francis Darwin notes in The life and letters of Charles Darwin, including an autobiographical chapter (1887), a major motivation was the apparently unlikely collision between the study of flowers and of natural selection. As Francis puts it: As soon as the idea arose that the offspring of crossfertilisation is, in the struggle for life, likely to conquer 167

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the seedlings of self-fertilised parentage, a far more vigorous belief in the potency of natural selection in moulding the structure of flowers is attained.

But even great scientists need their share of luck, and Darwin describes in his book how the original discovery of the importance of cross-fertilisation was largely accidental: For the sake of determining certain points with respect to inheritance, and without any thought of the effects of close interbreeding, I raised close together two large beds of self-fertilised and crossed seedlings from the same plant of Linaria vulgaris.To my surprise, the crossed plants when fully grown were plainly taller and more vigorous than the self-fertilised ones.

But why was he surprised? He had noted the ‘endless beautiful contrivances’ by which almost all plants ensured cross-fertilisation, and he of all people appreciated that natural selection doesn’t do anything so consistently without a very good reason. The answer is simply that he hadn’t appreciated just how important cross-fertilisation was: It often occurred to me that it would be advisable to try whether seedlings from cross-fertilised flowers were in any way superior to those from self-fertilised flowers. But as no instance was known with animals of any evil appearing in a single generation from the closest possible interbreeding, that is between brothers 168

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Common toadflax (Linaria vulgaris), the plant that first alerted Darwin to the importance of cross-fertilisation, drawn in 1796.

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and sisters, I thought that the same rule would hold good with plants; and that it would be necessary at the sacrifice of too much time to self-fertilise and intercross plants during several successive generations, in order to arrive at any result. I ought to have reflected that such elaborate provisions favouring cross-fertilisation, as we see in innumerable plants, would not have been acquired for the sake of gaining a distant and slight advantage, or of avoiding a distant and slight evil. Moreover, the fertilisation of a flower by its own pollen corresponds to a closer form of interbreeding than is possible with ordinary bi-sexual animals; so that an earlier result might have been expected.

Once his observations of Linaria had alerted him to how rapid and obvious were the negative consequences of self-fertilisation, ‘My attention was now thoroughly aroused’, and ‘I therefore determined to begin a long series of experiments with various plants, and these were continued for the following eleven years’. The results of these long years of work are exhaustively reported in his book, and Darwin issues the usual health warning that these chapters were likely to prove useful to any insomniacs among his readers: ‘Anyone not specially interested in the subject need not attempt to read all the details.’ He worked on morning glory, pinks, foxglove, cabbage, mullein, toadflax, violets, beans, peas, hibiscus, 170

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lobelias, passion flower, broom, tobacco, cowslip and many others. Crossed and selfed plants were carefully measured, and in some cases weighed, and Darwin gave a sample of his results to Francis Galton for his opinion of the reliance that could be placed on the differences between the two groups. Galton was a polymath in the

Sir Francis Galton, photographed in the 1850s or early 1860s.

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true sense of the word; in addition to being one of the fathers of modern statistics, he invented – and published in the journal Nature – a new way of cutting a cake to solve the problem ‘given a round tea-cake of some 5 inches across, and two persons of moderate appetite to eat it, in what way should it be cut so as to leave a minimum of exposed surface to become dry?’ You don’t see papers like that in Nature these days. Galton’s analysis of his data would today be regarded as somewhat rudimentary. However, it reassured Darwin ‘that I have by no means exaggerated the superiority of the crossed over the self-fertilised plants’. Often this superiority was remarkable. Cross-fertilised broom flowers produced twice as many seeds as selfed flowers, those seeds were heavier, and the plants grown from them were both taller and more likely to flower. Darwin also noted that the disadvantages of selfing were often dependent on the environment; for example, the true extent of the inferiority of selfed plants might only be revealed when they were exposed to competition or a stress such as a hard winter.

 Darwin and the gardeners – part 2 As much as Darwin relied on his own observations and experiments, he was in constant communication with other scientists and naturalists. Naturally, in his work on plants he also corresponded with gardeners, and 172

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they in turn were grateful to him for bringing some scientific rigour to an occupation that had previously suffered from at least its fair share of mumbo-jumbo (and, I would add, still does). Against this background, Darwin’s work on cross-fertilisation transformed plant breeding practically overnight. Even if you were aware that self-fertilisation was usually harmful, it was easy to misunderstand why this was so. For example, it was widely believed, and not just by would-be plant breeders, that the evils of selffertilisation or inbreeding proceeded from, as Darwin put it,‘the result of the increase of some morbid tendency or weakness of constitution common to the closely related parents’. But his careful experiments persuaded Darwin that this was nonsense; selfed or inbred offspring were weak because self-fertilisation itself was injurious, and not because of any weakness in the parent(s). The practical consequences, to those wide awake enough to perceive them, were crucial; you couldn’t get round the problems of self-fertilisation or inbreeding simply by making sure you started with a healthy parent. Maxwell T. Masters, editor of the Gardeners’ Chronicle, put it like this: The injury from the self-fertilisation of plants, as well as from too close breeding in animals, does not, according to Mr Darwin, depend on any tendency to disease or weakness of constitution common to related parents. 173

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On the other hand, the advantages of cross-fertilisation depend on the ancestors of the parent-plants having been exposed to different conditions, or from their having been intercrossed with individuals thus exposed. Thus is justified that common practice with horticulturists of obtaining seeds from different localities, and which have been grown under different conditions, so that the error and evil consequences of raising plants for a long succession under the same conditions may be avoided. … Bearing in mind the immense importance of the subject to raisers of new varieties, or to the growers of old ones, who are lamenting over the vanished constitution of roses, or the sterility or bad setting of grapes, cucumbers, strawberries, or what-not, it must be obvious how very valuable the record of such a series of experiments, carried on so patiently for so many years, must be.

 The genetics of self-fertilisation So, as Darwin and at least some of his readers appreciated, the advantages of cross-fertilisation arose from bringing together individuals that were (as we would recognise today) genetically distinct. Yet, in those pre-Mendelian days, no-one knew what was actually going on. In these passages from Cross and self-fertilisation, Darwin’s puzzlement is palpable: It is obvious that the exposure of two sets of plants during several generations to different conditions

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can lead to no beneficial results, as far as crossing is concerned, unless their sexual elements are thus affected. Plants which have been propagated for some generations under different climates or at different seasons of the year transmit different constitutions to their seedlings. Under such circumstances, the chemical constitution of their fluids and the nature of their tissues are often modified. Whatever affects an organism in any way, likewise tends to act on its sexual elements. The benefits which so generally follow from a cross between two plants apparently depend on the two differing somewhat in constitution or character.

So Darwin knew that cross-fertilisation in itself wasn’t necessarily beneficial; the offspring were superior only if the cross united plants differed in ‘constitution or character’, and thus had different ‘sexual elements’, but he didn’t know what these were, where they resided, or how they became altered over time. In short, he was talking about genes, but before the word had been coined or even the concept recognised. This inevitable lack of any understanding of genetics was a pity, because it meant that Darwin was unable to interpret some of his own observations. For example, Darwin compared selfed and crossed plants of Ipomoea purpurea (morning glory), with the

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usual outcome: the crossed plants were superior. But when he repeatedly selfed the offspring for several generations, he observed a surprising and quite unexpected result: In the sixth self-fertilised generation of Ipomoea a single plant named the Hero appeared, which exceeded by a little in height its intercrossed opponent, a case which had not occurred in any previous generation. Hero transmitted the peculiar colour of its flowers, as well as its increased tallness and a high degree of self-fertility, to its children, grandchildren, and great-grandchildren.

As is evident, Darwin was so surprised by this plant’s unexpected health that he gave it the nickname ‘Hero’. He speculated that sometimes, for reasons he was unable to explain, self-fertilisation was advantageous. To explain what was happening we have to understand why self-fertilisation or inbreeding are usually harmful. Many deleterious mutations are recessive, which means they can lurk undetected in large populations because they rarely end up in the same genome as another copy of the same gene, which is the only time they cause a problem. Inbreeding makes two recessive genes ending up in the same genome much more likely, but geneticists have now figured out that self-fertilisation or inbreeding might sometimes purge the bad genes – bad news for the unfortunate individuals that get purged, but good news for the lucky survivors. 176

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Darwin observed the purging of deleterious mutations in morning glory (Ipomoea purpurea), but lacked the knowledge of genetics to explain his observations.

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Darwin’s ‘Hero’ is now recognised as the first recorded observation of purging, but he was far too early to have any inkling of what he had found, and purging wasn’t properly understood until the 1990s.

 Self-incompatibility Was Darwin always right? No, he was not. He was aware that in some plants, the flowers were incapable of being fertilised by pollen from the same plant; even if such pollen was placed on the stigma, few or no seeds were produced. Yet he rejected the idea that this could have arisen by natural selection: ‘Nevertheless, the belief that self-sterility is a quality which has been gradually acquired for the special purpose of preventing selffertilisation must, I believe, be rejected.’ Self-sterility, he believed, was ‘incidental’. Darwin gives us a few reasons for this belief, but chiefly, I think, he was so mesmerised by the elaborate morphological adaptations for the prevention of self-fertilisation that he really didn’t see why self-sterility was necessary: ‘there are so many other means by which this result might be prevented or rendered difficult ... that self-sterility seems an almost superfluous acquirement for this purpose.’ We now know that self-sterility, or self-incompatibility as it is usually known, is an extremely common and important mechanism for the prevention of self178

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fertilisation. I’ll return to this topic when looking at Darwin’s book on different forms of flowers. Not only was Darwin not infallible, he could on occasion get two things wrong in the same sentence. Discussing the tendency of anemophilous (windpollinated) plants to have separate sexes, he suggests this might be due to ‘anemophilous plants having retained in a greater degree than the entomophilous [insect-pollinated] a primordial condition, in which the sexes were separated and their mutual fertilisation effected by means of the wind’. To be fair to Darwin, he was here only firing one of the opening shots in an argument that would rumble on for another century, with many authorities coming down on his side. But Darwin was wrong; very good evidence now points unambiguously to the earliest flowering plants being both hermaphrodite and insect-pollinated.

 Bees behaving badly It’s probably impossible to be interested in flowers and their pollination without also becoming captivated by the insects that are chiefly responsible, i.e. bees. So it’s no great surprise that the penultimate chapter of Cross and self-fertilisation is called ‘The Habits of Insects in Relation to the Fertilisation of Flowers’. This chapter reveals that Darwin was fascinated by the extent to which many tubular flowers have holes bitten in the 179

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base of the flower, allowing bees to ‘rob’ the flower of nectar without entering by the normal route. As he quickly ascertained, the culprits are bumblebees, which have powerful biting jaws. Honeybees do not, but they often exploit the holes made by bumblebees. As Darwin immediately saw, this behaviour raises all kinds of questions. To start with, how do the bees learn to do this? For as Darwin observed, once bees start robbing, they very quickly lose interest in entering flowers via the legitimate route:‘So persistent is the force of habit, that when a bee which is visiting perforated flowers comes to one which has not been bitten, it does not go to the mouth, but instantly flies away in search of another bitten flower.’ Recent research shows that bees are quick learners, but perhaps not in the way that you would expect. Bees do not learn to rob from observing the criminal behaviour of other bees, but they do learn from visiting flowers that have already been robbed, so that once bees experience robbed flowers, they are more likely to go on to bite new holes in intact flowers themselves. And in flowers that can be robbed from either the left or the right, such as hay rattle (Rhinanthus) and many salvias, bees also quickly learn which side to visit (if the flower is robbed already) or to make a new hole, so that all the flowers in a patch soon come to be robbed on the same side. 180

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A daffodil being ‘robbed’ of its nectar by an eastern carpenter bee. The hole in the base of the flower may have been made by another bee, or even by another species.

Other intriguing questions occurred to Darwin. It’s easy to see the point of robbery in flowers where the nectar is inaccessible, or found at the base of a long spur, but bees ‘often bite holes, although they could with very little more trouble obtain the nectar in a legitimate manner by the mouth of the corolla’. Many gardeners 181

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will have noticed the same thing; neither Abelia nor Kolkwitzia flowers are particularly deep or narrow, so the extra effort involved in entering the mouth of the flower must be small, but in my garden both are routinely robbed. Darwin reasoned that: ‘The motive which impels bees to gnaw holes through the corolla seems to be the saving of time, for they lose much time in climbing into and out of large flowers, and in forcing their heads into closed ones.’ Fair enough, once all or most flowers have been robbed, but what about the effort involved in making the holes in the first place? As Darwin observed: Nevertheless each bee before it has had much practice, must lose some time in making each new perforation, especially when the perforation has to be made through both calyx and corolla. This action therefore implies foresight, of which faculty we have abundant evidence in their building operations; and may we not further believe that some trace of their social instinct, that is, of working for the good of other members of the community, may here likewise play a part?

And never mind the bees, what about the effect on the plants? Darwin realised this could be disastrous: The plants, the fertilisation of which actually depends on insects entering the flowers, will fail to produce seed when their nectar is stolen from the outside; and

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even with those species which are capable of fertilising themselves without any aid, there can be no crossfertilisation, and this, as we know, is a serious evil in most cases.’

In short, there should be powerful selection for plants to find ways to reduce or mitigate the effects of robbing. Pondering these questions, Darwin made an observation that he thought might answer more than one of them: ‘Many years ago I was struck with the fact that humble-bees as a general rule perforate flowers only when these grow in large numbers near together.’ Naturally enough, large masses of flowers attract large numbers of pollinators, both legitimate and felonious, and so: ‘they find a large proportion of the flowers ... with their nectaries sucked dry. They thus waste much time in searching many empty flowers, and are led to bite the holes, so as to find out as quickly as possible whether there is any nectar present, and if so, to obtain it.’ It’s also possible that massed flowers encourage robbery because individual bees are more likely to benefit from holes made by other bees, and thus the whole thing becomes more of a cooperative enterprise. And it helps, as Darwin noted, that many of the bees foraging on a particular patch of flowers will be from the same nest and therefore siblings.

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If such mass larceny reduces or completely prevents seed production, then: As is so general throughout nature, there is a tendency towards a restored equilibrium. If a plant suffers from being perforated, fewer individuals will be reared, and if its nectar is highly important to the bees, these in their turn will suffer and decrease in number; but, what is much more effective, as soon as the plant becomes somewhat rare so as not to grow in crowded masses, the bees will no longer be stimulated to gnaw holes in the flowers, but will enter them in a legitimate manner. More seed will then be produced, and the seedlings being the product of cross-fertilisation will be vigorous, so that the species will tend to increase in number, to be again checked, as soon as the plant again grows in crowded masses.

It’s a neat hypothesis: common plants, with lots of flowers, are mercilessly robbed, produce fewer seeds and thus become less common. They are then less robbed, produce more seeds, become more abundant and robbery increases again, and so on in an endless cycle. It’s even susceptible to experimental test, although there’s no evidence that Darwin contemplated doing so. In fact, the words quoted above are his last on the subject, and the last words of Cross and self-fertilisation, apart from a final chapter of general conclusions.

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So was Darwin right? The first thing to say is that nectar robbing is today a large field of research, with a substantial literature and numerous academic careers devoted wholly or partly to its study. From which you will not be surprised to learn that the story of nectar robbing is not a simple one. In the first place, robbing is enormously variable from time to time and place to place; even species that are highly susceptible to robbing may often by chance escape entirely, which reduces the pressure to evolve counter-measures. Also, surprisingly, robbing does not always reduce seed production, and sometimes can even increase it, for reasons too arcane to elaborate here. Nevertheless, there is pressure to reduce robbing, but this doesn’t always take the form you might expect. Armour-plating appears not to be an option – it simply doesn’t pay to try to make essentially flimsy, ephemeral structures like flowers bite-proof. But the time and effort involved in biting holes is only merited if the reward gained is worth it, so one option is to reduce the volume or concentration of nectar. Of course, this may discourage legitimate pollinators so it needs to be finely judged, but it can be done; the nectar of scarlet gilia (Ipomopsis aggregata) is dilute enough to deter nectarrobbing bumblebees, but concentrated enough to still attract (legitimate) hummingbird pollinators. Perhaps

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surprisingly, one of the best defences against nectar robbing seems to be simply packing flowers together in dense aggregations, which makes it difficult for robbers to access the base of the flower from outside. And new research continues to reveal surprising plant responses to nectar robbing. For example, the epidermal cells of leaves tend to be flat, but those of petals are often conical. Partly this helps the flower to look brighter; conical cells act as a lens that focuses light into the vacuole (containing the anthocyanin pigment), which increases the intensity of the colour and also scatters reflected light more efficiently than a flat surface (a mutant antirrhinum with flat cells looks strangely pale and washed-out). But conical cells also provide a better surface for bees to grip with their feet, so plants that have made the transition from bee to bird pollination have all lost their conical epidermal cells, making the petal surface more slippery and therefore robbery by bees more difficult. Similarly, in bee-pollinated plants, the part of the flower vulnerable to nectar robbing, usually the base, also generally has flat epidermal cells. But in one respect Darwin was certainly right; subsequent studies all bear out his observation that lots of flowers per unit area leads to more robbery, so it’s entirely possible that nectar robbing can be added to the long list of checks and balances that tend to prevent any individual plant from taking over the world. 186

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 A family affair If you visit Darwin’s family home, Down House in Kent (as you should), you will inevitably take a quick stroll round the sandwalk, Darwin’s ‘thinking path’. At the junction where the path divides to circle Sandwalk Wood, there is a large ash tree. It was at the foot of this ash tree on 8 September 1854 that young George Darwin, then aged nine (and clearly a chip off the old block), saw several bumblebees, all males of the garden

Circuits of Sandwalk Wood were part of Darwin’s daily routine at Down House. The map shows his observations of the routes of patrolling male bumblebees.

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bumblebee (Bombus hortorum), briefly pause and buzz before flying off through the ‘crutch’ between the two large trunks of the ash tree. Darwin (Charles, that is) was intrigued, as he was by almost any piece of unexplained natural history. His work on plant fertilisation had already led him to take an interest in the behaviour of bees when visiting flowers, and it’s a short step from there to an interest in bees for their own sake. Over the next seven years, Darwin intermittently observed the bees’ behaviour, establishing that the bees patrolled a standard route, always pausing at the same spots for a quick buzz before moving on. As he wrote in his account: The routes remain the same for a considerable time, and the buzzing places are fixed within an inch. I was able to prove this by stationing five or six of my children each close to a buzzing place, and telling the one farthest away to shout out ‘here is a bee’ as soon as one was buzzing around.The others followed this up, so that the same cry of ‘here is a bee’ was passed on from child to child without interruption until the bees reached the buzzing place where I myself was standing.

His assistants in this work, along with George, were Willy (William Erasmus), Etty (Henrietta), Franky (Francis), Lenny (Leonard) and possibly Bessy (Elizabeth); today an academic faced with a similar task would employ a posse of undergraduates. 188

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Because all the bees were males, Darwin suspected the patrolling and buzzing behaviour was connected with attracting or finding mates, as it certainly is. But he did not see any queens or evidence of mating, and to this day mating in bumblebees remains elusive. He also wondered how all the bees knew the location of the ‘buzzing places’, writing in the margin of his notes: ‘How on earth do bees coming separately out of nest discover same place, is it like dogs at cornerstones?’ We now know that it is like dogs at cornerstones (or lampposts anyway), and that the bees mark the buzzing places by painting a pheromone from a gland in their heads on to a leaf or twig. But how the routes persist from one year to the next (since no male bee survives the winter) is unknown. In 1861, on holiday in Torquay, Darwin observed white-tailed bumblebees (Bombus lucorum) patrolling, and we now know that all species of bumblebee show the same behaviour, but tend to fly at different altitudes, presumably to avoid getting in each other’s way; garden bumblebees just happen to fly at a convenient height for human observation. In a photograph taken in the 1870s by Darwin’s son Leonard, the ‘crutch ash’ at Down is clearly visible. It’s still there today, but one of its two trunks has been felled, so it’s not quite the landmark it once was. 189

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 The curious primrose Published in seventy-two parts between 1777 and 1798, William Curtis’s Flora Londinensis is regarded as one of the foremost eighteenth-century illustrated floras. It contains beautiful illustrations of both the whole plant and dissected flowers of primrose (Primula vulgaris). The text reads: While we are thus describing the varieties to which this plant is subject, it may not be amiss to observe that the stamina also vary greatly in their situation, being sometimes found low down in the tube of the blossom, sometimes at its mouth, in the former instance the pistil which varies also in length shows its round stigma, and with its attendant style looks like a pin stuck in the centre of the flower; such flowers in the Polyanthus are termed pin-eyed, while those in which the anthers close the mouth of the tube, are called thrum-eyed, and this latter appearance in the opinion of the florist is an essential requisite in a good flower.

This may not be the first record that primrose has two distinct kinds of flowers, but it is one of the first, several years before Darwin was born. It’s also probably the first written use of the terms ‘pin-eyed’ and ‘thrum-eyed’. Pin-eyed makes intuitive sense, as the description above makes plain: the style and stigma of pin-eyed flowers do look like a pin inserted into the centre of the flower. But thrum-eyed? In The different forms of flowers, Darwin 190

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explains: ‘In Johnson’s Dictionary, thrum is said to be the ends of weavers’ threads; and I suppose that some weaver who cultivated the polyanthus invented this name, from being struck with some degree of resemblance between the cluster of anthers in the mouth of the corolla and the ends of his threads.’ This use of thrum is still extant,

Primrose (Primula vulgaris) pictured in William Curtis’s Flora Londinensis.

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according to my Shorter Oxford Dictionary, which is perhaps surprising as it’s not a word you would expect to know unless acquainted with a weaver. So, long before Darwin took an interest in them, Curtis (and others) had noticed flowers with different lengths of styles (now known as heterostyly), and correspondingly varied stamens. But why did the primrose have them? As Darwin noted, hardly anyone had previously thought them of any interest at all: ‘This difference has hitherto been looked at as a case of mere variability.’ Indeed Linnaeus, the father of modern plant nomenclature, was specifically of the view that ‘Varietates levissimas non curat botanicus’ – ‘the botanist is not concerned with slight variations’. Linnaeus even used Primula as an example of the tendency of flower enthusiasts to focus on insignificant floral details that no sensible botanist would consider important. One or two earlier botanists had, to be sure, suspected that the two forms of flowers must have some function, but were at a loss as to what that might be. As Darwin noted: This difference between the two forms has attracted the attention of various botanists, and that of Sprengel [Kurt Sprengel, German botanist and physician], in 1793, who, with his usual sagacity, adds that he does not believe the existence of the two forms to be accidental, though he cannot explain their purpose. 192

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I have to say that you can see why Linnaeus might have been unwilling to waste his time on ‘slight variations’. In the Flora Londinensis quote above, it’s apparent that gardeners, for no very obvious reason, considered thrum flowers superior to pins. In the first edition of The Gardener and Practical Florist, an article of 1843 lays down the law on the subject: ‘Some Polyanthus show the pistil, and are called pin-eyed; these are considered worthless.’ Harsh words indeed, especially when you consider (as Darwin was to show) that if you want any seeds, you need both thrum and pin. But to be fair to Linnaeus, primroses are prone to exhibit floral variation that really is of no great interest, other than to the collector of oddities: colours from almost white to deep yellow or even pink; flowers on a stalk, like a cowslip; double flowers; Jack-in-the-green, where the normal calyx is replaced by a ruff of tiny leaves; and hose-in-hose, in which a second flower grows through the centre of the first. But Darwin knew heterostyly was not ‘mere variability’. If it was, why was every plant either pin or thrum, with no trace of intermediates? And why – as he quickly established – did every population seem to contain the two morphs in approximately equal proportions? No, heterostyly bore all the hallmarks of a product of natural selection – of something with a purpose. But what was that purpose? 193

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 Peculiar primulas By the time Darwin published The different forms of flowers in 1877, he had been working on heterostyly for many years. He originally thought that the two forms of primrose flowers represented a stage in the evolution of separate sexes from a hermaphrodite ancestor; thus, although both forms had male and female sexual organs, one was on its way to becoming exclusively male, the other female: The first idea which naturally occurred to me was, that this species was tending towards a diœcious condition; that the long-styled plants, with their longer pistils, rougher stigmas, and smaller pollen-grains, were more feminine in nature, and would produce more seed;— that the short-styled plants, with their shorter pistils, longer stamens and larger pollen-grains, were more masculine in nature.

But Darwin soon satisfied himself that this couldn’t be true because both morphs produced plenty of viable seeds; in an 1861 letter to Asa Gray, he had already concluded that both forms of flower are hermaphrodite, and that ‘The pollen of A is fitted for stigma of B & conversely’. Which, in a nutshell, sums up the matter; one flower form (pin) has anthers halfway up the flower tube, clearly producing pollen intended for the other form, which has a stigma that’s also halfway up the flower tube. The other (thrum) has anthers at the top of 194

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Heterostyly in cowslip (Primula veris). Pin-eyed (left) and thrum-eyed (right) flowers, from Darwin’s book The different forms of flowers on plants of the same species.

the tube; its pollen is obviously intended for the stigma of pin flowers, also at the top of the tube. I say obviously because it seemed obvious to Darwin; natural selection didn’t arrive at something like heterostyly without a good reason. But he quickly set about discovering exactly what was going on, first in cowslip (Primula veris), then in other heterostylous primula species and finally in another member of the same family, the water violet (Hottonia palustris). 195

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To prove his point, Darwin conducted careful experimental crosses, both legitimate (pollen from short anthers to short style, or long anthers to long style) and illegitimate (short to long, or vice versa). In every case the result was the same – legitimate crosses produced more seeds, sometimes dramatically more. Darwin was impressed: From the facts now given the superiority of a legitimate over an illegitimate union admits of not the least doubt; and we have here a case to which no parallel exists in the vegetable or, indeed, in the animal kingdom. The

Cowslip flowers, illustrating legitimate and illegitimate pollen transfer. From Darwin’s book The different forms of flowers on plants of the same species.

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individual plants of the present species, and as we shall see of several other species of Primula, are divided into two sets or bodies, which cannot be called distinct sexes, for both are hermaphrodites; yet they are to a certain extent sexually distinct, for they require reciprocal union for perfect fertility. As quadrupeds are divided into two nearly equal bodies of different sexes, so here we have two bodies, approximately equal in number, differing in their sexual powers and related to each other like males and females.

It was yet another example, in addition to all those already explored in Cross and self-fertilisation, of an adaptation that had evolved to ensure crossfertilisation.

 Beyond primula But Primula and its relatives was far from the end of the story. If heterostyly was such a good idea, surely there must be other examples besides Primula and related genera? There were. Darwin noted several species of flax (Linum) with heterostyly, and conducted the usual crosses, legitimate and illegitimate, with the usual results. Close observation of pollen in Linum grandiflorum also revealed why; successful delivery of sperm to egg requires a pollen tube to grow down through the style to the ovary, and Linum pollen on the ‘wrong’ stigma 197

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either failed to germinate at all, or the pollen tube made little progress: Taking fertility as the criterion of distinctness, it is no exaggeration to say that the pollen of the long-styled Linum grandiflorum (and conversely that of the other form) has been brought to a degree of differentiation, with respect to its action on the stigma of the same form, corresponding with that existing between the pollen and stigma of species belonging to distinct genera.

Darwin also investigated heterostyly in lungwort (Pulmonaria), buckwheat (Fagopyrum), Forsythia and many others, including several members of the Rubiaceae (the coffee and bedstraw family). He wasn’t always able to conduct experiments, and in some cases had access only to dried specimens sent to him by correspondents. But whenever he was able to carry out experimental crosses, the story was the usual one. In short, heterostyly isn’t exactly common, but it is widespread.

 Darwin and the gardeners – part 3 Primulas were popular garden plants, and the early nineteenth century saw the establishment of ‘Societies of Florists’, dedicated to the cultivation of ‘Auriculas, Pinks, and Carnations’. Apparently the societies established in Islington and Chelsea were ‘not only the 198

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most numerous in point of numbers, but likewise the most respectable in regard to the members composing them’. But respectable or not, those who had turned their attention to hybridising the species and breeding new cultivars had found primulas to be frustratingly uncooperative. One gardener at the time, Donald Beaton, even asserted that ‘the cultivated varieties of the Primrose and Polyanthus do not yield to the natural laws of cross-breeding’. Darwin’s book cut through the prevailing murk like a searchlight. The general relief, not unmixed with chagrin, that at last someone had figured out what was going on, was expressed as usual by Maxwell Masters of the Gardeners’ Chronicle: It was not without some sense of humiliation and of wasted opportunity that florists and horticulturists found that they had been pottering over ‘pin-eyes’ and ‘thrum-eyes’ for generations, without having the slightest notion of the significance of the variations in question. Even from the restricted point of view of the professed florist, the meaning of the formations in question, and their direct practical bearing on the cultivation and selection of the forms most in consonance with his arbitrarily assumed standard were entirely overlooked. So-called botanists were, with very few exceptions, not one whit better. They had been splitting hairs, counting spots, wrangling whether this was a species and that a 199

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variety, discussing whether there were two or fifty British representatives of a particular genus, and so on, without troubling themselves in the least about the causes of the variations they observed in such minuteness of detail.

 Two morphs good, three morphs better We now come to examples of heterostyly that, as Darwin noted, ‘In their manner of fertilisation ... offer a more remarkable case than can be found in any other plant or animal’. The classic example, celebrated in botany textbooks across the globe, is purple loosestrife (Lythrum salicaria). In Lythrum, Darwin noted: This plant exists under three female forms, which differ in the length and curvature of the style, in the size and state of the stigma, and in the number and size of the seed. There are altogether thirty-six males or stamens, and these can be divided into three sets of a dozen each, differing from one another in length, curvature, and colour of the filaments—in the size of the anthers, and especially in the colour and diameter of the pollengrains. Each form bears half-a-dozen of one kind of stamens and half-a-dozen of another kind, but not all three kinds. The three kinds of stamens correspond in length with the three pistils: the correspondence is always between half of the stamens in two of the forms with the pistil of the third form. 200

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Flowers of the three forms of purple loosestrife (Lythrum salicaria), showing where pollen must be transferred to ensure full fertility. From Darwin’s The different forms of flowers on plants of the same species.

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In functional terms: when all three hermaphrodites coexist, and pollen is carried from one to the other, the scheme is perfect; there is no waste of pollen and no false coadaptation. In short, nature has ordained a most complex marriagearrangement, namely a triple union between three hermaphrodites,—each hermaphrodite being in its female organ quite distinct from the other two hermaphrodites and partially distinct in its male organs, and each furnished with two sets of males.

It’s enough to make your head spin. And, as Darwin quickly realised, the experimental crosses required were much more complicated than in Primula: Nothing shows more clearly the extraordinary complexity of the reproductive system of this plant, than the necessity of making eighteen distinct unions in order to ascertain the relative fertilising power of the three forms.

Nevertheless, Darwin set to as usual, although even he realised that the work involved to do the job properly was prohibitive: As in fertilising flowers there will always be some failures, it would have been advisable to have repeated each of the eighteen unions a score of times; but the labour would have been too great; as it was, I made 223 unions, i.e. on an average I fertilised above a dozen flowers in the eighteen different methods. 202

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And it wasn’t always easy: In making eighteen different unions, sometimes on windy days, and pestered by bees and flies buzzing about, some few errors could hardly be avoided. One day I had to keep a third man by me all the time to prevent the bees visiting the uncovered plants, for in a few seconds’ time they might have done irreparable mischief.

But in the end, at least the results were gratifyingly simple. The six legitimate crosses, between anthers and styles of the same length, yielded on average more than twice the seeds of the twelve illegitimate crosses. In addition to this mass of detail, Darwin also made detailed observations of pollinator behaviour, noting exactly how the flowers were designed to ensure insects usually transferred legitimate pollen. Could natural selection have come up with something as weird as trimorphic heterostyly more than once? Apparently yes; Darwin investigated several species of Oxalis, with the usual result: legitimate cross good, illegitimate cross bad. But the most surprising example was the Brazilian water plant Pontederia. None of the other heterostylous plants of which Darwin was aware were monocotyledons, that large minority of flowering plants including everything from grasses and lilies to palms and orchids. But Pontederia was not only 203

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The Brazilian water plant Pontederia cordata is tristylous, like purple loosestrife.

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a heterostylous monocot, it was the most complicated, trimorphic variant.

 Chickens and eggs Darwin was a genius, and one measure of his genius was just how often he came up with the right answer to some very tough questions. But by another measure Darwin was even greater than that. It’s one thing to solve a problem that’s foxed everyone else, it’s quite another to come up with the tough question in the first place. The really great geniuses of history – Copernicus, Newton, Einstein, Alfred Wegener (plate tectonics) – all solved problems that no-one else had even noticed or, worse, recognised but refused to take seriously. In his work on heterostyly, Darwin solved a problem that hardly anyone else recognised. And modest as he was, Darwin was understandably chuffed by his achievement; as he remarked in his autobiography, ‘no little discovery of mine ever gave me so much pleasure as the making out the meaning of heterostyled flowers’. But, to an extent that he cannot have realised, Darwin’s work set in motion a debate, or in truth several debates, that are not fully resolved even today. Darwin was satisfied that heterostyly was one among many other adaptations that had evolved to promote

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cross-fertilisation. Everything tended to support that view; for example, as Darwin noted: Plants which are already well adapted by the structure of their flowers for cross-fertilisation by the aid of insects often possess an irregular corolla, which has been modelled in relation to their visits; and it would have been of little or no use to such plants to have become heterostyled. We can thus understand why it is that not a single species is heterostyled in such great families as the Leguminosæ, Labiatæ, Scrophulariaceæ, Orchideæ, &c., all of which have irregular flowers.

In short, heterostyly is an ingenious way of promoting cross-fertilisation, but it’s not the most obvious way to achieve that end, and certainly far from the most common. Modern work has entirely vindicated Darwin’s view of the function of heterostyly. But it has also raised questions about heterostyly that are not easily resolved. For example, as Darwin repeatedly demonstrated, ‘illegitimate’ crosses were less fertile than ‘legitimate’ ones – in all the heterostylous plants he investigated, the different morphs were entirely or partly physiologically incompatible (the physiology and genetics of such incompatibility are other active research areas). So, if outcrossing can be guaranteed by the simple inability of pollen to fertilise the ‘wrong’ stigma, why bother with all the complicated morphology as well? Or, to put 206

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it even more simply, why have two adaptations doing essentially the same job, when surely either would be enough on its own? The answer, it is now generally agreed, is that heterostyly does indeed make little difference to the female function of flowers. What it does do is make the male function more efficient, by increasing the precision of pollen dispersal, while at the same time (by keeping anthers and stigma well apart within a single flower) reducing the likelihood of self-pollination (and thus pollen wastage). Which still leaves the large-scale evolutionary question: if heterostyly is always, or at least usually, accompanied by incompatibility between the morphs, which evolved first? Darwin was far from sure: ‘This is a very obscure subject, on which I can throw little light, but which is worthy of discussion.’ But he suggested that the heterostylous morphology evolved first, with incompatibility then arising more or less by accident, but certainly being of no great importance: It is a more probable view that the male and female organs in two sets of individuals have been by some means specially adapted for reciprocal action; and that the sterility between the individuals of the same set or form is an incidental and purposeless result.

Modern opinion is that the incompatibility is not quite as incidental as Darwin thought, but the exact 207

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evolutionary sequence remains obscure, with strong opinions on both sides. But there is a recent clue, from a source unknown to Darwin, and investigated in detail only in the twenty-first century. As we’ve seen, the only heterostylous monocot known to Darwin was the Brazilian water plant Pontederia. But since Darwin’s time, heterostyly has been identified in several other plant families, and is now known to occur in daffodils (Narcissus), which are of course monocots. Not only that, but daffodil heterostyly is unusual (indeed downright weird) in two other respects. In the first place, distyly and tristyly both occur in the genus. Narcissus triandrus is tristylous and Narcissus albomarginatus is distylous, while the other sixty or so species lack heterostyly. Since these two daffodils are in different sections of the genus, it looks like heterostyly has evolved independently at least twice within the daffodils. Something else that Darwin would have been intrigued to discover, and most likely quite gratified too, is that unlike all the species he was able to investigate, the morphs in both species of heterostylous daffodil are sexually compatible; provided the pollen can reach the stigma, any morph can pollinate the other morph(s). In other words, the job of ensuring cross-fertilisation in heterostylous daffodils is done by heterostyly alone, unassisted by incompatibility. Which strongly suggests that Darwin might have been right all along. 208

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 Heterostyly, genes and supergenes Naturally, Darwin couldn’t even hazard a guess at the genetics of heterostyly. But he wasn’t too far out when he compared the two morphs in dimorphic heterostyly to males and females in species that have separate sexes. Gender is usually determined genetically and, in the system we’re most familiar with, because it occurs in humans and most other mammals, sex is determined by a pair of chromosomes, X and Y. The Y chromosome determines maleness, so XY is male, XX female. The same kind of inheritance, but involving a pair of genes (rather than whole chromosomes), one dominant, the other recessive, is commonly referred to as Mendelian, from Gregor Mendel’s work on peas. Geneticists now conventionally denote dominant genes by a capital letter, and recessive genes by a lower-case letter. So, for example, in Mendel’s peas, the gene for purple flowers (P) is dominant, and that for white flowers (p) is recessive. Plants inherit a copy of the gene (technically an allele) from each parent, and as long as they have at least one copy of the dominant P gene, their flowers are purple. Thus PP and Pp plants have purple flowers, while pp plants have white flowers. When Mendel’s work was finally ‘rediscovered’ in 1900, heterostyly was seen as a textbook example. As William Bateson, who originally coined the term ‘genetics’, put it when writing in 1905: ‘In view of the results obtained 209

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by Darwin, Hildebrand and others, it seemed likely that the characters long-style and short-style, well known in Primulaceae and other orders, might have a Mendelian inheritance. Our experiments have shown that this is the case in P. sinensis, the short style being dominant, the long recessive.’ So heterostyly in Primula is a classic Mendelian character, with a dominant S (for short-style) gene and a recessive s (long-style) gene; thrum plants are either SS or Ss and pin plants are ss. Or is it? Heterostyly isn’t quite as simple as it appears, but the full story was revealed only in work published in 2016. In the first place, ‘S’ isn’t a single gene, it’s a collection of five genes that are so closely linked that they are always inherited together; geneticists call such things supergenes. In the second place, there is no ‘s’ gene; plants that lack the S supergene simply have nothing where it ought to be. The same work also reveals the S supergene to be ancient. In the familiar evolutionary story, in which there’s no point in inventing something new if you can modify something you already have, it originally regulated normal flower development. But around fifty million years ago, in an ancestor of Primula and related genera, this supergene was duplicated and the copy acquired a new job: heterostyly. There are two interesting postscripts to the unravelling of the genetics of heterostyly in Primula.The mastermind behind the research (and much else besides 210

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on the same subject) is Professor Philip Gilmartin from the University of East Anglia. In a press release to mark the publication, Gilmartin says: ‘This study answers some of the crucial questions that have been asked since Darwin’s time, and for me since I bought my first packet of Primula seeds twenty years ago.’ What were these seeds? Gilmartin tweeted seed merchants Thompson and Morgan to say that his discovery had all started with a packet of Primula seeds that he had bought from them in 1995, and he had a 1995 Thompson and Morgan catalogue to prove it.The variety in question was Primula ‘Blue Jeans’; apparently this particular F1 hybrid Primula variety was pivotal as it gave a very homogenous parent line on which to base his research.

 Darwin and Mendel Darwin and Mendel were working at the same time, but they never met, and as far as we can tell Darwin was completely unaware of Mendel’s work. But how close did Darwin come to discovering Mendel’s work? There is a popular story, perhaps designed to inject a little drama into this question, that Darwin had a copy of Mendel’s crucial paper in his library at Down House, but that the pages remained uncut and he never read it. But this appears to be an urban myth; no copy of the relevant journal is recorded in the catalogue of Darwin’s library, either now or at the time. 211

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Gregor Mendel, the Augustinian friar whose work on plant hybridisation has led to him being described as ‘the father of modern genetics’. Mendel and Darwin were contemporaries, but they never met, and Darwin was unaware of Mendel’s work.

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So what would have happened if Darwin had read Mendel’s paper remains one of the great ‘what-ifs’ of the history of science. We know Darwin saw the problem of inheritance very clearly; as he wrote in The Origin of Species: The laws governing inheritance are quite unknown; no one can say why a peculiarity in different individuals of the same species, or in individuals of different species, is sometimes inherited and sometimes not so; why the child often reverts in certain characters to its grandfather or grandmother or other more remote ancestor; why a peculiarity is often transmitted from one sex to both sexes, or to one sex alone, more commonly but not exclusively to the like sex.

Since Mendel’s work contained exactly the answer (or at least an answer) to these questions, it’s hard to imagine that Darwin wouldn’t have realised its significance. Mendel’s work might therefore not have languished in obscurity for thirty years, the eventual synthesis of evolutionary biology and genetics could have occurred much sooner, and essentially the whole history of biology might have been quite different. Mendel, for his part, was naturally familiar with Darwin’s work, but didn’t make the connection. But then Mendel was a careful and patient experimenter; Darwin was a genius.

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CHAPTER

5

The Mysteries of the Cabbage Patch The variation of animals and plants under domestication (1868)

E

ven after publishing The Origin of Species in 1859, Darwin continued to pile up new evidence in support of the ‘laws of nature’ he had outlined in the first edition: modification, the struggle for existence, survival of the fittest, and – especially – gradual evolution. By its sixth edition, published in 1872, The Origin had increased in size by a third, and much of the new material was botanical. 214

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Darwin’s six books devoted entirely to plants were essentially a by-product of this enormous botanical enterprise. In addition to these works, he also published The variation of animals and plants under domestication, a compendium of observations that essentially adds up to an immense appendix to chapter one of The Origin of Species. In that work, he says, the reader ‘has to take many statements on trust’, but here at last is everything you might possibly want to know on at least one subject considered only relatively briefly there: the parallel between ‘natural’ and ‘human’ selection: Man, therefore, may be said to have been trying an experiment on a gigantic scale; and it is an experiment which nature during the long lapse of time has incessantly tried. Hence it follows that the principles of domestication are important for us. The main result is that organic beings thus treated have varied largely, and the variations have been inherited.

Indeed the term ‘natural selection’ itself comes directly from the idea that if biological variation can be selected by humans, as it so clearly has, then surely the natural environment can do exactly the same, especially if given an unimaginably longer timescale: The term is so far a good one as it brings into connection the production of domestic races by man’s power of selection, and the natural preservation of varieties and species in a state of nature. 215

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And, he is careful to point out, there is no need to imagine that variation is created by this process; all that is necessary is selection: It is an error to speak of man ‘tampering with nature’ and causing variability. If organic beings had not possessed an inherent tendency to vary, man could have done nothing. He unintentionally exposes his animals and plants to various conditions of life, and variability supervenes, which he cannot even prevent or check.

The variation of animals and plants under domestication covers, as its title asserts, both plants and animals, but here we are concerned only with the botanical half. It is also a rather different book from the six we have looked at already, in that no great scientific principle is at stake. Variation under domestication is simply saying: the important argument is in The Origin of Species, and if you want all the evidence in support of that argument, well, here it is – in spades. Darwin often advised his readers that not all the detail in his books was strictly necessary for those who wanted to cut to the chase, and here his advice to those of a hasty disposition is clear: Whenever I have found it necessary to give numerous details, in support of any proposition or conclusion, small type has been used. The reader will, I think, find this plan a convenience, for, if he does not doubt the conclusion or care about the details, he can easily pass them over. 216

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Even so, it would be a mistake to ignore Variation under domestication completely, if only because its impact on the science of horticulture was far-reaching.

 Fruit, veg and flowers Darwin realised that studying the variation and origins of cultivated plants faced some formidable obstacles: I shall not enter into so much detail on the variability of cultivated plants, as in the case of domesticated animals. The subject is involved in much difficulty. Botanists have generally neglected cultivated varieties, as beneath their notice. In several cases the wild prototype is unknown or doubtfully known; and in other cases it is hardly possible to distinguish between escaped seedlings and truly wild plants, so that there is no safe standard of comparison by which to judge of any supposed amount of change. Not a few botanists believe that several of our anciently cultivated plants have become so profoundly modified that it is not possible now to recognise their aboriginal parentforms. Equally perplexing are the doubts whether some of them are descended from one species, or from several inextricably commingled by crossing and variation.

Or, as Darwin put it in a letter to Hooker after reviewing his notes on vegetables and fruit-trees: ‘awful work it is drawing any conclusions’. 217

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Some species and varieties of cultivated brassicas, none of which look much like their wild ancestors.

218

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You have been warned. Nevertheless, some principles were clear. For example, however much the object of selection came to vary as a result of that selection, parts that were not selected tended to remain the same. So although Darwin was impressed by the staggering amount of variation that selection has revealed in the edible, vegetative bits of the humble cabbage – everything from Brussel sprouts to cauliflower and kohl rabi – their flowers, seed pods and seeds vary hardly at all: What a contrast in the amount of difference is presented if, on the one hand, we compare the leaves and stems of the various kinds of cabbage with their flowers, pods, and seeds, and on the other hand the corresponding parts in the varieties of maize and wheat! The explanation is obvious; the seeds alone are valued in our cereals, and their variations have been selected; whereas the seeds, seed-pods, and flowers have been utterly neglected in the cabbage, whilst many useful variations in their leaves and stems have been noticed and preserved from an extremely remote period, for cabbages were cultivated by the old Celts.

He was also surprised how quickly this variation could be selected: ‘With respect to the radish, M. Carrière, by sowing the seed of the wild Raphanus raphanistrum in rich soil, and by continued selection during several generations, raised many varieties, closely 219

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like the cultivated radish (R. sativus) in their roots.’ To this day the origin of the cultivated radish remains a mystery; it has been grown and eaten for more than four thousand years, and is unknown as a wild plant. Maybe our remote ancestors had as little trouble as M. Carrière in turning an unappetising weed into a tasty addition to a salad? Moving on from cabbages, Darwin noted that it wasn’t the only species of Brassica to have been domesticated: The other cultivated forms of the genus Brassica are descended, according to the view adopted by Godron and Metzger, from two species, B. napus and rapa; but according to other botanists from three species; whilst others again strongly suspect that all these forms, both wild and cultivated, ought to be ranked as a single species.

Darwin wasn’t the first – or the last – to be confused by brassicas. In the first place, if one of Brassica napus and Brassica rapa is rape (canola in N. America), common sense says it surely ought to be Brassica rapa, but in fact it’s Brassica napus. And as for the debate about one species, or two, or three, the right answer is about one and a half, since rape isn’t even a proper species – it’s originally a hybrid between Brassica oleracea (cabbage) and Brassica rapa (turnip). It also exists only in cultivation, and is unknown as a genuine wild plant. 220

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As for marrows and squashes, it was impossible to tell anything about the cultivated plants our ancestors have left us with: Six species are now recognised in the genus Cucurbita; but three alone have been cultivated and concern us, namely, C. maxima and pepo, which include all pumpkins, gourds, squashes, and the vegetable marrow, and C. moschata. These three species are not known in a wild state.

It is fortunate that Darwin had plenty of space at Down.To give just one example of his almost incredible industry, he grew fifty-four varieties of gooseberry alone. This allowed him to say with some confidence that, in accordance with the principle that only the specific object of selection varies, the fruit varied a good deal, but the flowers were mostly indistinguishable. Mind you, it could have been worse; as Darwin noted The Catalogue of the Horticultural Society for 1842 gives 149 varieties, and the lists of the Lancashire nurserymen are said to include above 300 names. In the ‘Gooseberry Grower’s Register’ for 1862 I find that 243 distinct varieties have won prizes at various periods …

Darwin was fortunate (or unfortunate, depending on your point of view) to be writing at the height of the Victorian craze for gooseberry growing in the English north and midlands. The RHS Plant Finder now lists fewer than twenty varieties. 221

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Gooseberries are still grown at Down House, but as the present head gardener reminded me, all the varieties grown by Darwin were probably highly susceptible to American gooseberry mildew, which arrived in Europe at the start of the twentieth century.Today it’s really only worth growing modern resistant varities; sadly, ‘Roaring Lion’, ‘Highwayman’ and ‘Henderson’s Porcupine’ are probably gone forever. Garden flowers were hardly any better, and perhaps even worse: I shall not for several reasons treat the variability of plants which are cultivated for their flowers alone at any great length. Many of our favourite kinds in their present state are the descendants of two or more species crossed and commingled together, and this circumstance alone would render it difficult to detect the difference due to variation. For instance, our Roses, Petunias, Calceolarias, Fuchsias,Verbenas, Gladioli, Pelargoniums, &c., certainly have had a multiple origin.

You can almost feel the relief when Darwin came across something whose parentage was – perhaps – reasonably well understood. He started out with high hopes for pansies: The history of this flower seems to be pretty well known; it was grown in Evelyn’s garden in 1687; but the varieties were not attended to till 1810–1812, when Lady Monke, together with Mr. Lee, the well-known 222

THE VARIATION OF ANIMALS AND PLANTS ...

Wild pansy or heart's ease (Viola tricolor), one of several ancestors of the cultivated garden pansy.

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nursery-man, energetically commenced their culture; and in the course of a few years twenty varieties could be purchased.

But things quickly got out of hand, and by 1835 ‘a book entirely devoted to this flower was published, and four hundred named varieties were on sale’. You can almost feel Darwin’s early optimism draining away: But when I came to enquire more closely, I found that, though the varieties were so modern, yet that much confusion and doubt prevailed about their parentage. Florists believe that the varieties are descended from several wild stocks, namely, V. tricolor, lutea, grandiflora, amœna, and altaica, more or less intercrossed. And when I looked to botanical works to ascertain whether these forms ought to be ranked as species, I found equal doubt and confusion.

 Darwin and the gardeners – part 4 It mattered not a jot that Variation under domestication contained no great scientific advance; variation under domestication was what gardening was all about, and the reception in the Gardeners’ Chronicle was ecstatic: Written in admirable English, using no scientific terms but such as are comprehensible to men of fair education, lucidly arranged, and indexed with scrupulous care, there is not a gardener in the country who has any taste for the history or theory of his art but will peruse 224

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it with pleasure and profit, and find it difficult to say whether he values it more as a storehouse of facts [you can say that again] or as an incitement to observe and to think. Is his employer a sportsman? he will find in Mr Darwin’s pages such information regarding dogs and horses, their breeds and individualities, as never entered the brain of the gamekeeper, equerry, or master of the hounds. Is he a farmer? here are anecdotes and observations regarding cattle, pigs, sheep, and goats, which no professional breeder can match for number or truth, and which too few of these will believe or care about, not because they are not true, but because most so-called practical men take no interest in animals beyond what immediately concerns themselves. Is my lady a fowl fancier, or has she an aviary? her gardener will here find a wealth of information on domesticated birds of all sizes, voices, and uses, from the canary bird and peacock to the turkey and goose. Lastly, do his master’s children seek his advice about their rabbits, pigeons, honey bees, goldfish, or silkworms? If they do, here are curiosities of natural history about each and all, treated with masterly skill and originality.

Good stuff indeed, but many a sportsman or fowl fancier, incited by such a review into making a purchase, will probably have woken from a deep slumber in a fireside armchair, wondering what hit them after having run head first into Darwin’s ‘storehouse of facts’. It also speaks volumes about Darwin’s difficulty in drawing 225

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any conclusions about the origins and evolution of cultivated plants that even a review in a gardening magazine is all about dogs, sheep, canaries and goldfish. And, to venture a small comment on social history, it’s interesting that in 1868 the default assumption was that a ‘gardener’ was in the employ of his master or my lady. I wonder, too, how many of ‘his master’s children’ today keep silkworms, or even goldfish? Only a few months after the publication of Variation under domestication, the Royal Horticultural Society announced the formation of its Scientific Committee, charged with promoting and encouraging ‘the application of physiology and botany to purposes of practical culture, and to originate experiments which may assist in the elucidation of horticultural subjects’. Darwin was one of the committee’s founding members, as was Herbert Spencer (coiner of the term ‘survival of the fittest’). Other members of that first committee who will be familiar to modern gardeners included Robert Fortune, the plant hunter, and James Bateman, creator of the famous garden at Biddulph Grange.

226

UNDER DOMESTICATION

Afterword

D

arwin was beavering away on sundews, climbing plants and orchids around a century and a half ago, which seems almost unimaginably remote in our age of increasingly rapid technological and scientific progress. It was a different world – if Darwin wanted to work after dusk, it was by candlelight or oil lamp; if he wanted to travel to London, the journey was at least partly by horse-drawn coach. The recent science we have looked at also reflects this huge gulf; often carried out on plants unknown to Darwin, using technologies he couldn’t have imagined, and published in journals founded to cater for entirely new scientific disciplines. And yet the ideas in Darwin’s books are surprisingly current, and the questions he asked (and frequently answered) would be familiar to the denizens of 227

 AFTERWORD

any modern botanical research laboratory. Today’s researchers may be a long way down some fairly serpentine byways, but many of those byways began with an idea or observation that intrigued Darwin. Thus it was on account of his botanical work that Joseph Hooker offered the opinion that Darwin was ‘without doubt ... the first naturalist in Europe, indeed ... as great as any that ever lived’. Despite all this, although we all know Darwin (or think we do), we know him for one thing: The Origin of Species. The concession to plants on Darwin’s main Wikipedia entry is half a sentence on The power of movement in plants, and its only mention of botany concerns his son Francis. So what should they know of Darwin who only The Origin know? Surprisingly little, it turns out. I’ve tried in this book to put that right. Not to put Darwin the botanist front and centre, because that place will always (and rightly) belong to Darwin the author of The Origin of Species, but at least to prevent Darwin’s botany from slipping off the pages of history entirely. I hope I’ve succeeded, and that discovering some of Darwin’s other achievements, and where they have led, has been enjoyable as well as informative. I thought I would conclude with a couple of quotes from Francis Darwin’s recollections of his father’s 228

 AFTERWORD

botanical work, which seem to me to sum up Charles Darwin better than anything else: To the end of his life he never made any pretence to be a botanist, or at best ‘one of those botanists who do not know one plant from another,’ a saying, attributed to Nägeli, which he was fond of quoting. Thus, too, he wrote to Asa Gray on being elected to the Botanical Section of the French Institute: ‘It is rather a good joke that I should be elected in the Botanical Section, as the extent of my knowledge is little more than that a daisy is a compositous plant, and a pea a leguminous one ... He continued to study the means of fertilization of Orchids, &c., principally because of his irresistible desire to understand the machinery of living things. It is true that in elucidating the machinery he supplied the most brilliant evidence in favour of the validity of natural selection as the great moulding force in Nature. But I do not think this was his object, it was rather a by-product of work carried on for the love of doing it.

And what better reason is there for doing anything?

229

CHAPTER 5  SOURCES

Sources

GENERAL SOURCES

All Darwin’s written work can be found online at www.darwin-online.org.uk, and his correspondence at the Darwin Correspondence Project: www.darwinproject.ac.uk. The year 2009 marked both the bicentenary of Charles Darwin’s birth and 150 years since the publication of The Origin of Species. Not surprisingly, many scientific journals took the opportunity to publish retrospectives. Here is a selection of the botanical examples: Edwards, W. & Moles, A.T. (2009) ‘Re-contemplate an entangled bank: The power of movement in plants revisited’. Botanical Journal of the Linnean Society, 160, 111-118. Isnard, S. & Silk, W.K. (2009) ‘Moving with climbing plants from Charles Darwin’s time into the 21st century’. American Journal of Botany, 96, 1205-1221. Kutschera, U. & Briggs, W.R. (2009) From Charles Darwin’s botanical country-house studies to modern plant biology. Plant Biology, 11, 785-795. Weller, S.G. (2009) ‘The different forms of flowers – what have we learned since Darwin?’ Botanical Journal of the Linnean Society, 160, 249–261.

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 SOURCES

Whippo, C.W. & Hangarter, R.P. (2009) ‘The “sensational” power of movement in plants: a Darwinian system for studying the evolution of behavior’. American Journal of Botany, 96, 2115-2127. CHAPTER ONE

For a nice overview of climbing plants see Gianoli, E. (2015) ‘The behavioural ecology of climbing plants’. AoB Plants, 7, plv013. That the great majority of twining plants twine in a righthanded helix is shown in Edwards, W., Moles, A.T., & Franks, P. (2007) ‘The global trend in plant twining direction’. Global Ecology and Biogeography, 16, 795-800. Self/non-self discrimination in Cayratia japonica is described in Fukano,Y. & Yamawo, A. (2015) ‘Self-discrimination in the tendrils of the vine Cayratia japonica is mediated by physiological connection’. Proceedings of the Royal Society B:Biological Sciences, 282, 139-145. An old but good paper on the physiology of tendrils in climbing plants is Jaffe, M.J. & Galston, A.W. (1968) ‘Physiology of tendrils’. Annual Review of Plant Physiology, 19, 417-434. The role of G-fibres in tendrils is described in Bowling, A.J. & Vaughn, K.C. (2009) ‘Gelatinous fibers are widespread in coiling tendrils and twining vines’. American Journal of Botany, 96, 719-727. Three papers on the complexities of glue in ivy: Lenaghan, S.C., Burris, J.N., Chourey, K., Huang,Y., Xia, L., Lady, B., Sharma, R., Pan, C., LeJeune, Z., Foister, S., Hettich, R.L., Stewart, C.N., Jr., & Zhang, M. (2013) ‘Isolation and chemical analysis of nanoparticles from

231

 SOURCES

English ivy (Hedera helix L.)’. Journal of the Royal Society Interface, 10, 20130392. Melzer, B., Steinbrecher, T., Seidel, R., Kraft, O., Schwaiger, R., & Speck, T. (2010) ‘The attachment strategy of English ivy: a complex mechanism acting on several hierarchical levels’. Journal of the Royal Society Interface, 7, 1383-1389. Xia, L., Lenaghan, S.C., Zhang, M., Wu,Y., Zhao, X., Burris, J.N., & Stewart, C.N., Jr. (2011) ‘Characterization of English ivy (Hedera helix) adhesion force and imaging using atomic force microscopy’. Journal of Nanoparticle Research, 13, 1029-1037. Climbing without glue is described in Seidelmann, K., Melzer, B., & Speck, T. (2012) ‘The complex leaves of the monkey’s comb (Amphilophium crucigerum, Bignoniaceae): a climbing strategy without glue’. American Journal of Botany, 99, 1737-1744. Monstera climbing is described in Strong, D.R.& Ray, T.S. (1975) ‘Host tree location behavior of a tropical vine (Monstera gigantea) by skototropism’. Science, 190, 804-806. Climbing in Syngonium is described in Ray, T.S. (1987) ‘Cyclic heterophylly in Syngonium (Araceae)’. American Journal of Botany, 74, 16-26. The discovery of leaf mimicry in the chameleon vine is described in Gianoli, E. & Carrasco-Urra, F. (2014) ‘Leaf mimicry in a climbing plant protects against herbivory’. Current Biology, 24, 984-987. Two papers on climbing in the scrambler Galium aparine: Bauer, G., Klein, M.-C., Gorb, S.N., Speck, T.,Voigt, D., & Gallenmueller, F. (2011) ‘Always on the bright side: the climbing mechanism of Galium aparine’. Proceedings of the Royal Society B:Biological Sciences, 278, 2233-2239.

232

 SOURCES

Goodman, A.M. (2005) ‘Mechanical adaptations of cleavers (Galium aparine)’. Annals of Botany, 95, 475-480. CHAPTER TWO

The following papers all contain useful information on movement in plants.Vogel’s papers are an excellent introduction to rapid movement in plants and animals: Dumais, J. & Forterre,Y. (2012) ‘“Vegetable Dynamicks”: The role of water in plant movements’. Annual Review of Fluid Mechanics, 44, 453-478. Forterre,Y. (2013) ‘Slow, fast and furious: understanding the physics of plant movements’. Journal of Experimental Botany, 64, 4745-4760. Hill, B.S. & Findlay, G.P. (1981) ‘The power of movement in plants: the role of osmotic machines’. Quarterly Reviews of Biophysics, 14, 173-222. Martone, P.T., Boller, M., Burgert, I., Dumais, J., Edwards, J., Mach, K., Rowe, N., Rueggeberg, M., Seidel, R., & Speck, T. (2010) ‘Mechanics without muscle: Biomechanical inspiration from the plant world’. Integrative and Comparative Biology, 50, 888-907. Morillon, R., Liénard, D., Chrispeels, M.J., & Lassalles, J.P. (2001) ‘Rapid movements of plants organs require solute-water cotransporters or contractile proteins’. Plant Physiology, 127, 720-723. Vogel, S. (2005) ‘Living in a physical world - II. The bio-ballistics of small projectiles’. Journal of Biosciences, 30, 167-175. Vogel, S. (2005) ‘Living in a physical world - III. Getting up to speed’. Journal of Biosciences, 30, 303-312.

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 SOURCES

Plant growth responses to light (phototropism) are reviewed in Christie, J.M. & Murphy, A.S. (2013) ‘Shoot phototropism in higher plants: new light through old concepts.’ American Journal of Botany, 100, 35-46. The remarkable leaning Cook pine is described in Johns, J.W.,Yost, J.M., Nicolle, D., Igic, B., & Ritter, M.K. (2017) ‘Worldwide hemisphere-dependent lean in Cook pines’. Ecology, 98, 2482–2484. The following are useful papers about movement in Mimosa pudica: Fleurat-Lessard, P., Frangne, N., Maeshima, M., Ratajczak, R., Bonnemain, J.L., & Martinoia, E. (1997) ‘Increased expression of vacuolar aquaporin and H+-ATPase related to motor cell function in Mimosa pudica L’. Plant Physiology, 114, 827-834. Gagliano, M., Renton, M., Depczynski, M., & Mancuso, S. (2014) ‘Experience teaches plants to learn faster and forget slower in environments where it matters’. Oecologia, 175, 63-72. Jensen, E.L., Dill, L.M., & Cahill, J.F., Jr. (2011) ‘Applying behavioral-ecological theory to plant defense: lightdependent movement in Mimosa pudica suggests a trade-off between predation risk and energetic reward’. American Naturalist, 177, 377-381. Kameyama, K., Kishi,Y.,Yoshimura, M., Kanzawa, N., Sameshima, M., & Tsuchiya, T. (2000) ‘Tyrosine phosphorylation in plant bending - puckering in a ticklish plant is controlled by dephosphorylation of its actin’. Nature, 407, 37-37.

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 SOURCES

Plant intelligence is discussed in the following: Calvo Garzon, P. & Keijzer, F. (2011) ‘Plants: Adaptive behavior, root-brains, and minimal cognition’. Adaptive Behavior, 19, 155-171. Trewavas, A.J. & Baluska, F. (2011) ‘The ubiquity of consciousness’. Embo Reports, 12, 1221-1225. Mancuso, S. & Viola, A. (2015) ‘Brilliant Green:The Surprising History and Science of Plant Intelligence’. Island Press, Washington DC. Gagliano, M. (2015) ‘In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants’. AoB Plants, 7. Gagliano, M.,Vyazovskiy,V.V., Borbély, A.A., Grimonprez, M., & Depczynski, M. (2016) ‘Learning by association in plants’. Scientific Reports, 6, 38427. Movement of sunflower heads is reviewed in Vandenbrink, J.P., Brown, E.A., Harmer, S.L., & Blackman, B.K. (2014) ‘Turning heads: The biology of solar tracking in sunflower’. Plant Science, 224, 20-26. The operation of the fern sporangium catapult is described in Noblin, X., Rojas, N.O., Westbrook, J., Llorens, C., Argentina, M., & Dumais, J. (2012) ‘The fern sporangium: a unique catapult’. Science, 335, 1322-1322. The operation of the horsetail spore is described in Marmottant, P., Ponomarenko, A., & Bienaimé, D. (2013) ‘The walk and jump of Equisetum spores’. Proceedings of the Royal Society of London B: Biological Sciences, 280, 20131465. The remarkable Nuytsia floribunda is described in Calladine, A. & Pate, J.S. (2000) ‘Haustorial structure and functioning of the root hemiparastic tree Nuytsia floribunda (Labill.) R.Br. and water relationships with its hosts’. Annals of Botany, 85, 723-731.

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CHAPTER THREE

Three excellent overviews of carnivorous plants are: Chase, M.W., Christenhusz, M.J.M., Sanders, D., & Fay, M.F. (2009) ‘Murderous plants: Victorian Gothic, Darwin and modern insights into vegetable carnivory’. Botanical Journal of the Linnean Society, 161, 329-356. Ellison, A.M. & Gotelli, N.J. (2001) ‘Evolutionary ecology of carnivorous plants’. Trends in Ecology & Evolution, 16, 623-629. Krol, E., Płachno, B.J., Adamec, L., Stolarz, M., Dziubinska, H., & Trebacz, K. (2012) ‘Quite a few reasons for calling carnivores “the most wonderful plants in the world”’. Annals of Botany, 109, 47-64. The mutualistic relationship between Roridula, bugs and spiders is described in Anderson, B. & Midgley, J.J. (2002) ‘It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant Roridula’. Oecologia, 132, 369-373. Studies on the glue of Roridula, and how bugs avoid it, are described in: Voigt, D. & Gorb, S. (2008) ‘An insect trap as habitat: cohesion-failure mechanism prevents adhesion of Pameridea roridulae bugs to the sticky surface of the plant Roridula gorgonias’. Journal of Experimental Biology, 211, 2647-2657. Voigt, D. & Gorb, S. (2010) ‘Desiccation resistance of adhesive secretion in the protocarnivorous plant Roridula gorgonias as an adaptation to periodically dry environment’. Planta, 232, 1511-1515. Voigt, D., Konrad, W., & Gorb, S. (2015) ‘A universal glue: underwater adhesion of the secretion of the carnivorous flypaper plant Roridula gorgonias’. Interface Focus, 5, 20140053.

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 SOURCES

The investigation of possible carnivory in the bird-catcher tree is described in Burger, A.E. (2005) ‘Dispersal and germination of seeds of Pisonia grandis, an Indo-Pacific tropical tree associated with insular seabird colonies’. Journal of Tropical Ecology, 21, 263-271. Convergent evolution in pitcher plants, together with recent work on Cephalotus, is described in Mithöfer, A. (2017) ‘Plant carnivory: pitching to the same target’. Nature Plants, 3, 17003. ‘Catapult tentacles’ in the Australian sundew, Drosera glanduligera, are described in Poppinga, S., Hartmeyer, S.R.H., Seidel, R., Masselter, T., Hartmeyer, I., & Speck, T. (2012) ‘Catapulting tentacles in a sticky carnivorous plant’. Plos One, 7, e45735. The Utricularia trap is described in Vincent, O., Weisskopf, C., Poppinga, S., Masselter, T., Speck, T., Joyeux, M., Quilliet, C., & Marmottant, P. (2011) ‘Ultra-fast underwater suction traps’. Proceedings of the Royal Society of London B: Biological Sciences, 278, 2909-2914. Carnivory in Genlisea is described in Barthlott, W., Porembski, S., Fischer, E., & Gemmel, B. (1998) ‘First protozoa-trapping plant found’. Nature, 392, 447. The mutualism between Bornean Nepenthes and tree shrews is described in: Greenwood, M., Clarke, C., Lee, C.C., Gunsalam, A., & Clarke, R.H. (2011) ‘A unique resource mutualism between the giant Bornean pitcher plant, Nepenthes rajah, and members of a small mammal community.’ PloS One, 6, e21114. Moran, J.A., Clarke, C., Greenwood, M., & Chin, L. (2012) ‘Tuning of color contrast signals to visual sensitivity maxima of tree shrews by three Bornean highland Nepenthes species’. Plant signaling & behavior, 7, 1267-70.

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The mutualism between Nepenthes and bats is described in: Grafe, T.U., Schoener, C.R., Kerth, G., Junaidi, A., & Schoener, M.G. (2011) ‘A novel resource-service mutualism between bats and pitcher plants’. Biology Letters, 7, 436-439. Jones, G. (2015) ‘Sensory biology: acoustic reflectors attract bats to roost in pitcher plants’. Current Biology, 25, R609-R610. The partnership between the Bornean pitcher plant and ants is described in Thornham, D.G., Smith, J.M., Grafe, T.U., & Federle, W. (2012) ‘Setting the trap: cleaning behaviour of Camponotus schmitzi ants increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata’. Functional Ecology, 26, 11-19. For viscoeleastic polymers in the traps of Nepenthes pitcher plants, see Bonhomme,V., Pelloux-Prayer, H., Jousselin, E., Forterre,Y., Labat, J.-J., & Gaume, L. (2011) ‘Slippery or sticky? Functional diversity in the trapping strategy of Nepenthes carnivorous plants’. New Phytologist, 191, 545-554. Chemical warfare in Nepenthes madagascariensis is described in Ratsirarson, J. & Silander, J.A. (1996) ‘Structure and dynamics in Nepenthes madagascariensis pitcher plant microcommunities’. Biotropica, 28, 218-227. The remarkable ant-capture mechanism of Nepenthes gracilis is described in Bauer, U., Paulin, M., Robert, D., & Sutton, G.P. (2015) ‘Mechanism for rapid passive-dynamic prey capture in a pitcher plant’. Proceedings of the National Academy of Sciences of the United States of America, 112, 13384-13389. The underground traps of Philcoxia are described in Pereira, C.G., Almenara, D.P., Winter, C.E., Fritsch, P.W., Lambers, H., & Oliveira, R.S. (2012) ‘Underground leaves of Philcoxia trap and digest nematodes’. Proceedings of the National Academy of Sciences of the United States of America, 109, 1154-1158.

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 SOURCES

CHAPTER FOUR

Another ‘2009 review’ describes the pollination of the orchid Angraecum sesquipedale by the hawkmoth Xanthopan morganii var. praedicta: Micheneau, C., Johnson, S.D., & Fay, M.F. (2009) ‘Orchid pollination: from Darwin to the present day’. Botanical Journal of the Linnean Society, 161, 1-19. For the reception of Darwin’s work in the British horticultural press, I am indebted to Elliott, B. (2010) The reception of Charles Darwin in the British horticultural press. Royal Horticultural Society, London. A few interesting papers on nectar robbing: Irwin, R.E. & Maloof, J.E. (2002) ‘Variation in nectar robbing over time, space, and species’. Oecologia, 133, 525533. Irwin, R.E., Adler, L.S., & Brody, A.K. (2004) ‘The dual role of floral traits: Pollinator attraction and plant defense’. Ecology, 85, 1503-1511. Mayer, C., Dehon, C., Gauthier, A.-L., Naveau, O., Rigo, C., & Jacquemart, A.-L. (2014) ‘Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp lusitanicum’. Evolutionary Ecology, 28, 669-685. Rojas-Nossa, S.V., Sanchez, J.M., & Navarro, L. (2016) ‘Effects of nectar robbing on male and female reproductive success of a pollinator-dependent plant’. Annals of Botany, 117, 291-297. Rojas-Nossa, S.V., Sanchez, J.M., & Navarro, L. (2016) ‘Nectar robbing: a common phenomenon mainly determined by accessibility constraints, nectar volume and density of energy rewards’. Oikos, 125, 1044-1055. Moyroud, E. & Glover, B.J. (2017) ‘The physics of pollinator attraction’. New Phytologist, 216, 350-354.

239

 SOURCES

Dave Goulson (2014) discusses Darwin’s work on bees, and much else besides, in his excellent book A Sting in the Tale (Vintage, London). For an excellent short review of the evolution and significance of heterostyly, see Barrett, S.C.H. (1990) ‘The evolution and adaptive significance of heterostyly’. Trends in Ecology & Evolution, 5, 144-148. The history of the observation of heterostyly in Primula is described in Gilmartin, P.M. (2015) ‘On the origins of observations of heterostyly in Primula’. New Phytologist, 208, 39-51. Bateson’s original 1905 paper is Bateson, W. & Gregory, R.P. (1905) ‘On the inheritance of heterostylism in Primula’. Proceedings of the Royal Society of London B: Biological Sciences, 76, 581-586. Heterostyly in daffodils is reviewed in Barrett, S.C.H. & Harder, L.D. (2005) ‘The evolution of polymorphic sexual systems in daffodils (Narcissus)’. New Phytologist, 165, 45-53. The discovery of the heterostyly supergene in Primula is described in Li, J., Cocker, J.M., Wright, J., Webster, M.A., McMullan, M., Dyer, S., Swarbreck, D., Caccamo, M., Oosterhout, C.V., & Gilmartin, P.M. (2016) ‘Genetic architecture and evolution of the S locus supergene in Primula vulgaris’. Nature Plants, 2, 16188. CHAPTER FIVE

For the reception of Darwin’s work in the British horticultural press, I am again indebted to Elliott, B. (2010) The reception of Charles Darwin in the British horticultural press. Royal Horticultural Society, London.

240

Photo Credits Photo credits

Photos in the book are copyright of the following sources. Every effort has been made to contact copyright holders but if any have been missed, please contact the publishers so information can be corrected on future editions. Introduction p.12 Darwin’s barnacles (from vol 2 of Darwin’s Monograph of the sub-class Cirripedia; public domain); p.17 Victor Eustaphieff painting (Getty Images); p.21 sundew (from Darwin’s Insectivorous plants; public domain). Chapter One p.30 runner bean and black bryony (Ken Thompson); p.33 Wisteria sinensis on Down House (Ken Thompson; p.40 vine tendril (from Darwin’s The movements and habits of climbing plants; public domain); p.44 Cayratia japonica (Shutterstock); p.50 white bryony tendril (from Darwin’s The movements and habits of climbing plants; public domain); p.53 Virginia creeper tendril (from Darwin’s The movements and habits of climbing plants; public domain); p.57 Monkey’s comb (floradelcaribeilustrada.blogspot.com); p.60 Syngonium podophyllum (Alamy Stock Photos); p.64 Chameleon vine (Ernesto Gianoli); p.67 Galium aparine (Karl Niklas).

241

 PHOTO CREDITS

Chapter Two p.74 Darwin’s experiments (Bio 275); p.78 leaning Cook pine (Matt Ritter); p.81 Mimosa pudica (public domain; p.89 sunflowers (North Carolina Department of Transportation/ Wikipedia); p.97 fern leptosporangium (www.78stepshealth. us); p.100 horsetail spore (1896 illustration; public domain/ Wikimedia Commons). Chapter Three p.105 sundew (public domain/Pinterest); p.108 Roridula gorgonias (Wikimedia Commons); p.112 bird-catcher tree (David Eickhoff/Wikimedia Commons); p.117 Nepenthes distillatoria (Paxton’s Magazine of Botany/Wikimedia Commons); p.119 Cephalotus follicularis (1847 illustration; public domain); p.122 Venus fly-trap (public domain/ Pinterest); p.124 Drosera glanduligera (from Catapulting Tentacles in a Sticky Carnivorous Plant by Poppinga et al.); p.127 Aldrovanda vesiculosa (from Darwin’s Insectivorous Plants; public domain); p.130 Butterwort (from Dr. Otto Wilhelm Thomé’s Flora von Deutschland, 1885; public domain); p.133 Bladderwort (Wikimedia Commons); p.135 Utricularia bladder (André de Kesel/Getty Images); p.137 Genlisea violacea (Noah Elhardt/Wikimedia Commons); p.140 Nepenthes veitchii (Louis van Houtte, Flore des serres et des jardins de l’Europe, 1845/Wikimedia Commons); p.145 Hardwicke’s Woolly Bat (Minden Pictures/Alamy Stock Photo); p.148 Nepenthes gracilis (Bauer, U., B. Di Giusto, J. Skepper, T.U. Grafe & W. Federle 2012/Wikimedia Commons); p.151 Darlingtonia californica (Noah Elhardt/ Wikimedia Commons). Chapter Four p.159 Epipactis palustris (cpctv/Wikimedia Commons); p.163 Darwin’s moth (Thomas William Wood, 1867; Wikimedia Commons); p.166 Joseph Hooker (Wellcome Images/ 242

 PHOTO CREDITS

Wikimedia Commons); p.169 Linaria vulgaris (Johann Georg Sturm from Deutschlands Flora in Abbildungen, 1796; Wikimedia Commons); p.171 Francis Galton (from The Life, Letters and Labours of Francis Galton. Karl Pearson 1914; Wikimedia Commons); p.177 Morning glory (from Favourite flowers of garden and greenhouse by Edward Step, 1897; Wikimedia Commons); p.181 Daffodil being ‘robbed’ (Marvin Smith/ Wikimedia Commons); p.187 Sketch of part of the grounds at Down House (from darwin-online.org.uk); p.191 Primrose (from William Curtis Flora Londinensis, 1775; public domain); p.195 Heterostyly in cowslip (from Darwin’s The different forms of flowers on plants of the same species; public domain); p.196 Cowslip flowers (from Darwin’s The different forms of flowers on plants of the same species; public domain); p. 201 Heterostyly in purple loosestrife (from Darwin’s The different forms of flowers on plants of the same species; public domain); p.204 Pontederia cordata (from: Les liliacées by PierreJoseph Redouté, Paris, 1802–1816; Wikimedia Commons); p.212 Gregor Mendel (from Mendel’s Principles of Heredity: A Defence by William Bateson, 1902; Wikimedia Commons). Chapter Five p.218 Cultivated brassicas (The Natural History Museum/ Alamy Stock Photo); p.223 Wild pansy (Carl Lindman, 1917–26; Wikimedia Commons).

243

Thanks

First of all, thanks to the great man himself. Admiring Darwin is more or less compulsory for academic biologists, but paying detailed attention to what he actually wrote is often not, and I don’t think I really appreciated Darwin until I started to read his original botanical work. Also profuse thanks to all the scientists whose work has enabled me to bring Darwin up to date. Some were consciously following in Darwin’s footsteps, some were not, but it’s been great fun following the Darwinian threads in so much recent research. I’ve done my best to cite all my important sources in the bibliography. A special thank-you to the Head Gardener of Down House, Antony O’Rourke, and volunteer Terry Pyle, who both gave up an afternoon to share not only their knowledge, but their obvious love for the place. Many, many thanks to Mark Ellingham of Profile Books, especially for persuading me to write the book that needed writing, rather than the one I might have written if left to myself. As usual, if this book is now any good, Mark can take much of the credit. Sincere thanks also to Henry Iles for design, Susanne Hillen for proofreading, Bill Johncocks for the index and Peter Dyer for the wonderfully lush cover. Thanks as ever to my friends and family who put up with me banging on about Darwin, and especially to Pat, Rowan and Lewis. 244

 INDEX

Index Italic page numbers refer to illustrations. Aside from The Origin of Species, books by Darwin are at ‘Darwin, Charles, publications’.

A action potentials .................................... 47 adaptations, beauty of... 24, 157, 168 adhesives, animal ................................... 55 adhesives, plant see plant glues Albany pitcher plant (Cephalotus follicularis) ......................... 118–21, 119 Aldrovanda (vesiculosa)........... 121, 123, 126–8, 127 alkaloids ........................................ 149, 154 amino acids D- and L- ..........................................35–6 substitutions, and carnivory ....... 120 Ampelopsis sp............................................ 49 Amphilophium crucigerum...... 56–7, 57 anemophily............................................ 179 Angraecum sesquipedale .........161–5 animals carnivory in plants and................. 103 parallels with ................. 42, 47, 76, 85 annual passion flower (Passiflora gracilis) .............................................. 39–40 anti-malarials, potential.................. 154 ants ............................ 146–8, 152–3, 152 apogeotropism ........................................ 77 see also gravity Araceae.......................................... 61–2, 66 Araucaria columnaris ............... 78, 78–9 Artemisia tridentata................................. 45 associative learning .............................. 84

Australia, carnivorous plants ...... 116, 118, 123–4 auxin .....................................................75, 91

B bactericides, from butterworts ... 129 barnacles .............................. 9–13, 12, 55 Bateman, James ........................ 162, 226 Bateson, William................................. 209 bats ............................................. 144–6, 145 Beaton, Donald ................................... 199 bees bumblebees ...............180, 185, 187–9 compromising experiments....... 203 nectar robbing ................... 180–6, 181 as pollinators .............................. 179–80 beetles .................................125, 127, 159 Bignonia capreolata............................ 55–6 bird-catcher tree (Pisonia brunoniana) ...............................111, 112 birds caught by pitcher plants .............. 139 as pollinators ...................... 165, 185–6 black bryony (Tamus communis) ....30 bladderworts ............... 13, 128, 131–8, 133, 135, 141, 152 underwater traps ................................. 19 Utricularia spp. ........ 133, 135, 136–8 Bombus hortorum .................................. 187 Bombus lucorum .................................... 189

245

 INDEX Boquila trifoliolata (chameleon vine) 18, 63–5, 64 brassicas Brassica napus, B. rapa and B. oleracea............................................... 220 variety of cultivated ... 218, 219–20 Brazil ....................... 155, 203, 204, 208 breeding see plant breeding Brilliant Green, by Stefano Mancuso ................................................. 87 bromeliads hosting bladderworts ..................... 136 water storage .............................. 111–12 Bryonia dioica ................................... 46, 50 bumblebees ................ 180, 185, 187–9 Burger, Alan .......................................... 111 ‘bushkiller’ ................................................44 butterworts (Pinguicula) .........128–31, 130, 155 Byblis ................................................. 115–16

C cabbages ................................................... 219 calcium, and signal transmission.. 47 Camponotus schmitzi.......................... 146 ‘carnivorous habitats’...103, 113–14, 155 carnivorous plants Aldrovanda ....................................... 126–8 of Australia ..................... 116, 118, 123 butterworts and bladderworts ........... 128–38 CD’s passion for ....... 13, 121, 141–2 Cephalotus ......................... 118–21, 119 classification..................... 115, 117–18 definition of carnivory ............ 106–7 disputed existence .............................. 19 evolution and genetic basis ....... 106, 113–15, 117, 120–2, 126, 155 part-time carnivory / protocarnivory........... 19, 107, 154

Philcoxia................................................. 155 pitcher plants ............................. 139–53 purpose of plant carnivory ... 103–6 size of insect prey ............................ 125 with sticky leaves ..................... 115–17 Triphyophyllum peltatum................... 19, 153–4, 154 Venus fly-trap as a one-off ... 121–6, 122 see also sundews (Drosera) Carrière, Élie-Abel .................. 219–20 catapult action of sporangia ..... 96–8 catapult tentacles of Drosera glanduligera..................................... 123–4 Cayratia japonica........................ 43–5, 44 cell shapes annular cells ................................... 96, 97 epidermal cells .................................. 186 cell walls and elastic energy ...95, 98 Cephalotus (follicularis) ............. 118–21 chameleon vine (Boquila trifoliolata) 18, 63–5, 64 chemical attractants / pheromones . 138, 149, 189 chemical communication .. 45, 63–5 Chilean glory flower (Eccremocarpus scaber) .................................................47, 56 chirality see handedness chitin digestion ........................ 121, 128 Christmas tree, Western Australian (Nuytsia floribunda) ................... 101–2 circadian clocks ................................ 9293 circumnutation...............................72, 87 Cirripedia (barnacles).... 9–13, 12, 55 climbing plants continuing relevance of CD’s work ..................................................... 16 Mivart’s objection to CD’s views .... 70 scrambling plants, hooked ........65–8

246

 INDEX sticky climbers / root climbers.. 29, 51–65 twining plants ............................... 24–36 using tendrils ................................ 36–51 clockwise and anticlockwise, as ambiguous ............................................. 30 cobra lily (Darlingtonia californica) ...... 149–151, 151 coleoptiles ................................... 73–5, 91 colour preferences .............62, 91, 144 compression wood ............................... 78 coniine...................................................... 149 Cook pines (Araucaria columnaris) ..... 78, 78–9 Coriolis effect ......................................... 31 corkscrew plants / traps..... 137, 138 cowslip (Primula veris) ......... 193, 195, 195–6 creeping fig (Ficus pumila) ............... 54 cross-fertilisation heterostyly and............................. 205–6 importance .....158–61, 167–74, 197 cross-vine (Bignonia capreolata) 55–6 cucumbers ........................................... 51–2 Cucurbita genus .................................... 221 Curtis, William ....... 122, 190–2, 191

D daffodils (Narcissus)................ 181, 208 darkness, growth toward............ 58–9, 61–2, 66 Darlingtonia ........................ 118, 149–51 D. californica ......................149–51, 151 Darwin, Charles attitude to botany.................... 11, 227 capacity for hard work .9, 167, 202, 221 obsessiveness ........................10, 13, 157 Darwin, Charles, correspondence letter to Charles Lyell.................... 142 letters to Asa Gray ...... 142, 194, 227

letters to Joseph Hooker14–15, 28, 157, 162 The Life and Letters of..., by Francis Darwin........................................ 167–8 Darwin, Charles, publications Beagle Diary......................................... 116 On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing (1862).... 156, 157–67 On the movements and habits of climbing plants (1865) .....23–4, 26, 29, 38–9, 40, 50, 53 The variation of animals and plants under domestication (1868)................ 215–16 Insectivorous Plants (1875) ............. 21, 103–4, 121–2, 141 The effects of cross and self-fertilisation in the vegetable kingdom (1876) ...... 156, 167–72, 174–5, 179, 184 The different forms of flowers on plants of the same species (1877) ..... 156, 190, 194, 200, 201 The Power of Movement in Plants (1880) .... 69, 71–2, 79, 81, 85, 87, 93, 114–15 see also Origin of Species Darwin, Francis. 11, 69, 104, 167–8, 188, 227 Darwin, George............................ 187–8 Darwin, Leonard ..................... 188, 189 Darwin, William, Henrietta and Elizabeth .............................................. 188 Darwin’s moth (Xanthopan morganii).................................... 163, 164 deceptive pollination .............. 159–60 design, evidence against ......... 37, 157 Dionaea muscipula (Venus fly-trap).... 13, 114–15, 121–3, 122 evolution ......................................... 125–6

247

 INDEX Dioncophyllaceae .............................. 155 dispersal of pollen ............................................... 207 of seeds ............................................. 8, 111 of spores................................................ 101 domestication and natural selection ............................................... 215 Down House garden Wisteria..................................... 32 greenhouse .......................................... 162 library..................................................... 211 painting set in ....................................... 17 sandwalk ............................................... 187 Drosera (individual species) D. glanduligera ..................... 123–4, 124 D. rotundifolia .................. 21, 105, 114 see also sundews Drosophyllum ......................................... 117

E Eccremocarpus scaber .......................47, 56 Echinocystis ................................................. 41 Ecuador....................................................... 29 elaters ........................ 99–101, 100, 125 Engler, Adolf ............................................60 Epipactis palustris .................................159 Equisetum.................................................100 Evelyn, John .......................................... 222 evolution CD’s gradualism ....... 69–70, 72, 104 co-evolution of orchids and pollinators ................................. 164–5 convergent evolution . 113, 118–21 evolution, independent of carnivory .......... 106, 113–15, 117, 120–2, 155 of heterostyly ................................ 207–8 of twining plants ................................. 34

F faeces as a nutrient..... 107, 109, 112, 143–4, 149 ferns, sporangia of ...... 95–9, 97, 101 fertilisation see cross-fertilisation; pollinators; self-fertilisation Ficus pumila ............................................... 54 flax (Linum)............................................ 197 Flora Londinensis, by William Curtis.............................. 190, 191, 193 Flora von Deutschland..., by Otto Wilhelm Thomé .............................130 flower stalks (peduncles) ......... 37, 40 flowers heterostyly ......... 192–5, 195, 197–8, 200, 203, 205–10 multiple origins of cultivated ... 222 nectar robbing ................... 180–6, 181 pin-eyed and thrum-eyed..... 190–1, 193–4, 195, 199, 210 flypaper plant (Roridula gorgonias).............................. 107–9, 108 Fortune, Robert ................................. 226 frogs ............................................................ 112

G g-fibres .................................................. 51–2 Gagliano, Monica ................................. 84 Galium aparine ...........................66–8, 67 Galton, Sir Francis........... 171, 171–2 The Gardener and Practical Florist193 Gardeners’ Chronicle ......... 165, 173–4, 199, 224 gardening assumptions about, in 1868 ....... 226 effect of CD’s Variation under Domestication ............................ 224–6 effect of CD’s work on crossfertilisation ................................ 172–4 effect of CD’s work on orchids......................................... 165–7

248

 INDEX effect of CD’s work on primulas................................ 198–200 evidence for natural selection ..................................... 15–16 geckos .......................................................... 54 The Genesis of Species, by St George Jackson Mivart .................................... 70 genetics of carnivory ................................... 120–4 CD’s ignorance of ......... 20, 175, 211 coinage of the term ....................... 209 cross- and self-fertilisation..... 174–8 gene purging................................. 176–8 of heterostyly ............................. 209–11 Genlisea.................................... 136–8, 155 G. violacea ............................................. 137 genome sizes ......................................... 138 Gerard, John, Herball, or Generall Historie of Plantes ................................ 88 Gilmartin, Philip ................................ 211 glues see plant glues gooseberries .................................... 221–2 goosegrass (Galium aparine) ..... 66–8, 67 grass coleoptile response to light......73–5 as a model organism ......................... 75 gravity effects ............................ 75–9, 78 Gray, Asa ...... 23–4, 66, 142, 194, 227 growth habit, changing ..................... 59

H handedness molecular asymmetry and ........35–6 in non-plant species .......................... 35 opposition in spiral contraction ....... 47–50 twining plants, examples of each ..... 18, 30 twining plants, preponderance.......... 34–6

Hardwicke’s woolly bat (Kerivoula hardwickii) ........................... 144–6, 145 haustoria .................................................. 102 hay rattle (Rhinanthus) .................... 180 heart’s ease (Viola tricolor) ..............223 Heliamphora ................................. 118, 143 Helianthus annuus ......................... 87–94 heliotropism ................. 88–91, 114–15 hemiparasites ........................................ 101 Hemiptera bugs .............. 107, 110–11 Herball, or Generall Historie of Plantes, by John Gerard ................. 88 herbivores defences against 63, 81, 83, 86, 121, 146–7 responses to............................................ 45 hermaphroditism ........ 179, 194, 197, 202 ‘Hero’ (morning glory) ....... 176, 178 heterophylly .......................................... 153 heterostyly beyond Primula ......197–8, 200, 203, 205–10 evolution ......................................... 207–8 genetics of ................................... 209–11 and incompatibility ................... 206–8 and pollen dispersal ........................ 207 Primula spp. ......................... 192–5, 195 trimorphic (tristyly) ..... 200–3, 204, 205, 208 homeopathy ............................................. 10 honeysuckle .....................................29, 35 Hooker, Sir Joseph Dalton appreciation of CD ................... 166–7 as CD’s botanical guide .................. 13 CD’s letters to 14–15, 28, 157, 162, 217 cited by CD........................................ 115 at Down House................................... 17 portrait .................................................. 166

249

 INDEX specimens supplied by ....... 116, 137, 162 work on Nepenthes .................. 139–41 hops .......................................................25, 32 horizontal gene transfer.................... 65 horsetail sporangia ................... 99–101 horticulture see gardening Hottonia palustris.................................. 195 Hydrangea anomala ssp. petiolaris .... 56 hydraulic / hydrostatic pressure.. 46, 82, 94, 98, 102

L

inbreeding, dangers..... 168, 171, 176 see also self-fertilisation inheritance, problem of ................. 213 insectivorous plants see carnivorous insects ants...........................146–8, 152–3, 152 beetles ...............................125, 127, 159 greasy protective layers ......... 110–11 moths ............................ 20, 163, 164–5 in orchid pollination ............. 157–67 size, taken by Drosera and Dionaea............................................. 125 see also bees intelligence in plants..... 20, 42, 84–7 distributed intelligence ................... 85 Ipomoea hederacea .................................... 62 Ipomoea purpurea................. 175–6, 177 Ipomopsis aggregata .............................. 185 irritability...........................................26, 39 ivy plant glues of................................. 17–18 as a root climber ......................... 52, 55

Lardizabalaceae....................................... 63 leaf shape, changing.....................59, 63 leaves adaptation for carnivory ... 106, 114, 121, 137, 153 adapted as tendrils .............................. 37 behaviour at night.............................. 81 following the sun ....................... 88–90 heterophylly ....................................... 153 hooked ..................................... 67–8, 154 mucronate............................................... 63 left-handed twiners ...... 30, 31–2, 35 legitimate and illegitimate crosses.... 206–7 Lythrum spp......................................... 203 Primula spp. ........................ 196, 196–7 Lentibulariaceae ........... 128, 136, 138 see also bladderworts; butterworts; Genlisea lianas ............................................ 29, 153–4 light sensitivity ......................... 73–5, 84 carnivorous plants ................... 114–15 colour of light ...................................... 91 growth toward darkness............58–9, 61–2, 66 lignification ........................................ 51–2 Linaria vulgaris .................. 168–70, 169 Lindley, John ......................................... 165 Linnaeus, on Primula.................. 192–3 Linnean Society, 1858 meeting ... 71 Linum (grandiflorum) .................... 197–8 longbows .................................................... 95 Lyell, Charles ............................... 17, 142 Lythrum salicaria ...... 200–3, 201, 204

K

M

Kerivoula hardwickii ........... 144–6, 145 Kew Gardens see Hooker, Sir Joseph

MacDougal, D T ................................... 41 maize ............................................................ 62 Mancuso, Stefano ................................. 87

I

250

 INDEX marsh helleborine (Epipactis palustris) ................................................159 Marshall, W............................................ 128 Masters, Maxwell T ......... 173–4, 199 Mendel, Gregor ... 174, 209–13, 212 Mendelian inheritance .......... 209–10 Michigan rose (Rosa setigera) .......... 66 micro-fibrils, in ivy.............................. 52 milk, curdling ....................................... 129 Mimosa pudica ......................... 79–84, 81 Mivart, St George Jackson ..... 69–70 The Genesis of Species ........................ 70 molecular asymmetry................... 35–6 Moles, Angela.......................................... 31 monkey’s comb (Amphilophium crucigerum) .................................56–7, 57 monocotyledons................ 203–5, 208 Monstera spp. .............................. 58–9, 61 morning glory (Ipomoea purpurea) .... 175–6, 177 morning glory, ivyleaf (Ipomoea hederacea) ................................................. 62 moths............................... 20, 163, 164–5 movement bladderworts, rapidity of ............. 135 N. gracilis pitcher lid .................. 151–3 sporangia, rapidity of ...................98–9 twisting movements of shoots..... 25 mud and seed dispersal.........................8 mutations deleterious ................................ 176, 177 recessive ............................. 176, 209–10 mutualism / symbiosis........ 109, 143, 146

N nanocomposites .................... 17–18, 54 Narcissus triandrus / N. albomarginatus.................. 181, 208 natural selection cross-fertilisation and .... 167–8, 178

evidence from carnivory ............ 104, 114, 118, 120 evidence from climbing plants ......... 23–4, 36 evidence from gardening ...... 15–16, 215 gradualism in .......... 7–8, 69–70, 157 heterostyly and............. 193, 195, 203 nectar robbing .................... 180–6, 181 nematodes .............................................. 155 Nepenthaceae ...................................... 139 Nepenthes spp. ... 117–18, 120, 140–3 N. attenboroughii................................. 139 N. bicalcarata...............................146, 148 N. distillatoria ...................................... 117 N. gracilis................................ 151–3, 152 N. hemsleyana ...................... 144–6, 145 N. lowii ................................................... 143 N. madagascariensis............................ 149 N. rajah................................................... 144 N. veitchii............................................... 140 nitrogen, detection by sundews ......... 104, 142 nutrients, and carnivory .... 103, 113, 155 Nuytsia floribunda.......................... 101–2

O orchids Angraecum sesquipedale .............. 161–5 deceptive pollination ............. 159–60 insect fertilisation .................... 157–67 marsh helleborine (Epipactis palustris)............................................ 159 pollination by moths ........................ 20 seed characteristics..................... 160–1 The Origin of Species expansion of successive editions ...... 214 predating CD’s botanical studies .. 12

251

 INDEX quotations .................8–10, 13, 69–70, 157–8, 213

P Pameridea roridulae / P. marthothii ..................... 107, 109–11 pansies ............................................222, 223 parapara (Pisonia brunoniana) ...... 111, 112 parasitism hemiparasites ...................................... 101 root parasitism .............................. 101–2 Paris japonica .......................................... 138 Parthenocissus quinquefolia ................. 38, 49, 53, 55–6 Passiflora coerulea ..................................... 41 Passiflora gracilis....................... 39–41, 46 passion flower, common (Passiflora coerulea)..................................................... 41 Paxton, Joseph, Magazine of Botany (1838) ....................................................117 peas response to stimuli ............................. 84 as tendril climbers .............................. 37 Pfeffer, Wilhelm ....................... 86–7, 93 Das Pflanzenreich....................................60 Phalaris canariensis.................................. 73 Phaseolus coccineus (runner bean)..30 pheromones........................................... 189 Philcoxia.................................................... 155 phototropins ............................................ 91 phylogeny, molecular.... 20, 115, 120 Piaget, Jean................................................ 86 pin-eyed flowers ......... 190, 193, 195, 199, 210 Pinguicula (vulgaris) ...... 128–31, 130, 155 Pisonia brunoniana ....................111, 112 pitcher plants ....................... 19, 139–53 Albany pitcher plant as unrelated.... 118–21, 119

ant symbiosis ................................. 146–8 genus Darlingtonia......... 149–51, 150 genus Nepenthes .............................. 117, 117–18, 120, 139–46, 140, 145, 140, 148–9, 151–3, 152 genus Sarracenia..... 114–15, 118–20, 139, 141, 143, 149 use of viscoelastic polymers... 148–9 plants convenience for experimentation... 11 uncertain origins of cultivated plants ................................................. 217 plant breeding effect of CD’s work on crossfertilisation ................................ 172–4 effect of CD’s work on primulas ..... 199–200 plant glues of creeping fig ...................................... 54 of ivy ......................................... 17–18, 54 as nanocomposites ............. 17–18, 54 of parapara ........................................... 111 of Roridula ................................... 109–11 sundew mucilage ............................. 110 plant hormones, auxin...............75, 91 plasmodesmata ........................................... 47 plate tectonics ............................................8 pollen dispersal .................................... 207 pollen tube growth..................... 197–8 pollinators beetles and crickets .............159, 165 birds ........................................ 165, 185–6 deceptive pollination ............. 159–60 insects, and legitimate pollen .... 203 insects as, for early plants ............ 179 insects as, for orchids ............. 157–67 sunflower rotation and ...............88–9 wind pollination (anemophily) 179 pollinia.................................... 159, 160–2 polymers, viscoelastic ................. 148–9

252

 INDEX Pontederia (cordata) . 203–5, 204, 208 primrose (Primula vulgaris).............. 20, 190–6, 191, 195, 198–9 Primula spp. frustration of plant breeders ............... 199–200 legitimate and illegitimate crosses... 196, 196–7, 203, 206 Primula ‘Blue Jeans........................... 211 Primula sinensis ..................................... 210 Primula veris (cowslip) ......... 193, 195, 195–6 Primula vulgaris (primrose) ............. 20, 190–6, 191, 195, 198–9 problem solving ..................................... 86 proteins a-helices as right-handed ............... 36 actin ........................................................... 47 associated with carnivory ........... 120 protocarnivory / part-time carnivory .......................... 19, 107, 154 purple loosestrife (Lythrum salicaria) 200–3, 201, 204

R radish (Raphanus raphanistrum and R. sativus) .................................... 219–20 ratchet action .......................................... 68 Rattus baluensis ..................................... 144 Ray, Thomas ............................................ 58 reaction wood .................................51, 77 recessive genes / mutations ........ 176, 209–10 reed canary grass (Phalaris canariensis)............................................... 73 ‘revolving nutation’ ............................. 72 right-handedness preponderance .................. 31–2, 34–6 right-handed twiners .............. 30, 31 root climbers/sticky climbers ...... 29, 51–65

roots awareness ................................................. 85 gravity effects ................................76–77 self- and non-self discrimination..... 42–3 Roridula genus .......109–11, 115, 118, 132 R. dentata .............................................. 107 R. gorgonias .......................... 107–9, 108 Rosa setigera ............................................... 66 roses, climbing .................................. 65–6 Royal Horticultural Society (RHS) ................................ 20, 221, 226 Royal Society.......................................... 80 runner bean (Phaseolus coccineus) ..30

S Sachs, Julius von ...................... 45–6, 72 sagebrush (Artemisia tridentata)...... 45 Sarracenia.......... 114–15, 118–20, 139, 141, 143, 149 S. flava .................................................... 149 S. purpurea ............................................ 141 scarlet gilia (Ipomopsis aggregata) 185 seed banks ....................................................9 seeds characteristics of orchid seeds ........... 160–1 from cross- and self-fertilisation....... 172 dispersal range ......................................... 8 proportion surviving ................ 14–15 self- and non-self discrimination physiological coordination explanation ............................... 43, 45 plant tendrils and roots ..............42–3 self-fertilisation disadvantages .............................. 168–74 occasional advantages .................... 176 self-incompatibility ................... 178–9 shoots, twisting movements ........... 25

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 INDEX shrews.................................................. 143–4 ‘sleep movements’ ........................81, 93 species discoveries since CD’s time .. 18–19 geographical distribution problem . 7–8 variety in turf........................................ 15 Spencer, Herbert ................................ 226 spiders ............................................ 125, 142 Synaema marlothi ............................... 109 spiral contraction, tendrils ..... 49–52, 53 spores and sporangia of ferns ............................ 95–8, 97, 101 of horsetails ................................. 99–101 Sprengel, Kurt...................................... 192 sticky climbers / root climbers ... 29, 51–65 stimuli, plant responses ....... 41, 75–6, 82–4 Strong, Donald ....................................... 58 the sun following ......................................... 88–91 and twining plants ............................. 31 sundews (Drosera) ........... 103–4, 110, 114–15, 129 CDs preoccupation with13, 141–2 D. glanduligera ..................... 123–4, 124 D. rotundifolia .................. 21, 105, 114 relationship to Aldrovanda ........... 126 relationship to Dionaea (Venus fly-trap)..................................121, 125 relationship to Nepenthes and Drosophyllum ................................. 117 relationship to Roridula ............... 107, 109–10, 115 sunflowers (Helianthus annuus)............ 87–94, 89 supergenes .............................................. 210 ‘survival of the fittest’ coinage... 226

symbiosis / mutualism........ 109, 143, 146 Synaema marlothi ................................. 109 Syngonium genus...........................60, 61

T tactile bleps ......................................... 46–7 Tamus communis ......................................30 technology unavailable to Darwin .. 17–19, 94, 98 high-speed cameras .........19, 98, 134 telecommunications cables .......... 102 temperature and tendril behaviour . 42 tendrils as adapted flower stalks ........... 37, 40 as adapted leaves.................................. 37 climbing plants using ............... 36–51 coiling mechanism........................45–6 discrimination by ..........................41–4 spiral contraction ........................ 47–52 tenacity and longevity ................38–9 touch sensitivity ............ 39–41, 46–7 tension wood........................................... 78 thinking ability in plants .................. 76 Thiselton-Dyer, William ............... 140 Thomé, Otto Wilhelm, Flora von Deutschland, Österreich und der Schweiz (1885) .................................130 thrum-eyed flowers ...190–1, 193–4, 195, 199, 210 toadflax, common (Linaria vulgaris).............................. 168–70, 169 touch sensitivity assumed, for twining climbers .... 26 of Drosera glanduligera..................... 123 of Mimosa pudica .......................... 79–80 of tendrils.......................... 39–41, 46–7 trees climbing plants on ........29, 58, 61–2 leaning and..................................... 77, 78

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 INDEX wood types................................51, 77–8 Trewavas, Anthony ............................... 86 triffids ........................................................ 114 Triphyophyllum peltatum ... 19, 153–4, 153–5, 154 Tronchet, Antonin................................ 41 trumpet creepers (Bignoniaceae) .............................. 55–6 Tupaia montana ............................... 143–4 turgor ........................................................... 94 twining plants ................................ 24–36 direction of twining..16–18, 29–36 independent evolution .................... 34 left- and right-handed twiners ....................................... 30, 31 origins..................................................72–3 support thickness ...........................27–9

U ultraviolet reflecting cells.............. 112 Utricularia spp. ..................... 135, 136–8 U. humboldtii ....................................... 136 U. vulgaris.............................................. 133

V Venus fly-trap (Dionaea muscipula) .... 13, 114–15, 121–3, 122 evolution ........................................... 125–6 vines adaptation for climbing .. 23, 37, 40 Cayratia japonica ..................... 43–5, 44 chameleon vine (Boquila trifoliolata) ..................... 18, 63–5, 64 Vitis spp ................................................... 37

Viola tricolor and other Viola species................................... 222–4, 223 Virginia creeper (Parthenocissus quinquefolia) ............38, 49, 53, 55–6 vision hypothesis ................................... 65 Vitis spp see vines volatile chemicals..........................45, 65

W walking, horsetail spores....... 99–100 Wallace, Alfred Russel.............71, 163 water in carnivorous habitats.................. 113 in maintaining turgor....................... 94 in Nuytsia root amputation........ 102 in rapid plant movements ..... 46, 82, 94, 96–8, 123 storage in bromeliads ............ 111–12 water loss and tendril coiling ..... 46, 51 water violet (Hottonia palustris) .. 195 waterwheel plant (Aldrovanda vesiculosa) ............................. 126–8, 127 white bryony (Bryonia dioica) 46, 50 wind pollination (anemophily). 179 Wisteria spp. (Wistaria in CD’s spelling) ............................ 18–19, 27–8 W. floribunda ......................................33–4 W. sinensis ........................................ 32, 33 Wood, Thomas ....................................163

X Xanthopan morganii var. praedicta ......... 163, 164

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