This page intentionally left blank Plants: Evolution and Diversity Plantsaresomuchpartofourenvironmentthatweoftentakethemfor granted,yetbeautiful,fascinatingandusefulplantsareeverywhere,from isolatedmosscoloniesonstonewallstovastcomplexcommunitieswithin tropical rainforests. How did this array of form and habitat come about, andhowdowehumansinteractwiththeplantkingdom?Thisbookpro- vides a refreshing and stimulating consideration of these questions and throwslightinanewwayonthecomplexity,ecology,evolutionanddevel- opmentofplantsandourrelationshipwiththem.Illustratedthroughout withnumerouslinediagramsandbeautifulcolourphotographs,thebook provides a unique source of information about the fascinating lives that plants lead and the way in which our lives are inextricably linked to theirs. It will be particularly useful to those seeking a more ecological andprocess-orientedapproachthanisavailableinothertextbooks. martin ingrouilleisaseniorlectureratBirkbeckCollege,Universityof London,whereheteachesbotany,genetics,ecology,biogeographyandevo- lutionandresearchestheevolutionaryecologyandsystematicsofplants. Hehastravelledwidelyduringthecourseofhisstudies,includingEurope, North and Central America, East Africa, South East Asia, Australia and New Zealand. He is author of the widely adopted textbook Diversity and EvolutionofLandPlants(1992)fromwhichthispresentbookhasbeendevel- oped. bill eddie is a tutor at the University of Edinburgh where he teaches botany, ornithology, evolution and geopoetics as part of the University’s Open Studies programme. His research focuses on the evolutionary ecol- ogy and systematics of plants and birds, and he has a particular interest in the history of botany, and in birds and wildlife in art. He has a long- term interest in the Campanulaceae, and did molecular research on this family at the University of Texas, Austin. He has travelled widely during the course of his career, including Europe, North and Central America, CentralandSouthernAfrica,SouthEastAsia,andAustralia,andhasheld afour-yearteachingpostattheUniversityofPapuaNewGuinea. Plants: Evolution and Diversity Martin Ingrouille School of Biological and Chemical Sciences, Birkbeck College, University of London Bill Eddie University of Edinburgh    Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo Cambridge University Press The Edinburgh Building, Cambridge  , UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridg e.org /9780521790970 © M. Ingrouille and W. Eddie 2006 This publication is in copyright. Subject to statutory exception and to the provision of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published in print format 2006 - ---- eBook (EBL) - --- eBook (EBL) - ---- hardback - --- hardback - ---- paperback - --- paperback Cambridge University Press has no responsibility for the persistence or accuracy of s for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Contents Preface pagevii Chapter 1 Process, form and pattern 1 1.1Living at the edge of chaos 1 1.2Process: the evolution of photosynthesis 9 1.3Form: the origin of complex cells 19 1.4Pattern: multicellularity in the algae 38 1.5What is a plant? 48 1.6Sub-aerial transmigration of plants 54 Further reading for Chapter 1 55 Chapter 2 The genesis of form 56 2.1Plant development 56 2.2Plant growth and differentiation 60 2.3The integration of developmental processes 75 2.4Cellular determination 81 2.5The epigenetics of plant development 87 2.6The theory of morphospace 94 Further reading for Chapter 2 95 Chapter 3 Endless forms? 97 3.1The living response 97 3.2The nature of evolutionary processes 104 3.3Order, transformation and emergence 108 3.4Macromutation and evolutionary novelty 112 3.5Unity and diversity; constraint and relaxation 115 3.6The phenotype 116 3.7Variation and isolation 120 3.8Conceptualising plant form 123 Further reading for Chapter 3 133 Chapter 4 Sex, multiplication and dispersal 135 4.1The yin and yang of reproduction 135 4.2Sex 136 4.3Dispersal 140 4.4From sex to establishment 150 4.5The dispersal mechanisms 161 4.6The diversity of flowers 174 Further reading for Chapter 4 190 vi CONTENTS Chapter 5 Ordering the paths of diversity 191 5.1The phylogeny of plants 191 5.2The non-flowering plants 197 5.3Class Magnoliopsida -- flowering plants 223 Further reading for Chapter 5 251 Chapter 6 The lives of plants 252 6.1Plant diversity around the world 252 6.2Aquatic and wetland plants 254 6.3Halophytes 260 6.4Plant of low-nutrient conditions 269 6.5Plants of moist shady habitats (sciophytes) 282 6.6Epiphytes, hemi-epiphytes and vines 286 6.7Grasslands and savannas 295 6.8Plants of cold or hot arid habitats 299 6.9Island floras 308 Further reading for Chapter 6 316 Chapter 7 The fruits of the Earth 317 7.1Exploiting plants 317 7.2Plants for food 321 7.3Plants for craft and fuel 332 7.4Plants for the soul 338 7.5The scientific improvement of plants 356 7.6The flowering of civilisation 361 Further reading for Chapter 7 370 Chapter 8 Knowing plants 371 8.1The emergence of scientific botany 371 8.2Evolutionary botany 388 8.3Phylogeny, genetics and the New Systematics 403 8.4The green future 419 Further reading for Chapter 8 424 Index 426 Preface Dancing is surely the most basic and relevant of all forms of expression. Nothing else can so effectively give outward form to an inner experience. Poetry and music exist in time. Painting and architecture are a part of space. But only the dance lives at once in both space and time. In it the creator and the thing created, the artist and the expression, are one. Each participant is completely in the other. There could be no better metaphor for an understanding of the . . . cosmos. LyallWatson(GiftsofUnknownThings) The metaphor of dance is a very apt way to portray the unfolding andincreasingcomplexityofplant-lifeonEarth.Thedanceofplants is the dance of plant form in space and time. From a reductionist pointofview,theconversionofsolarenergyiswhatplantsarereally all about, either at the level of the individual, or the community, or even in the characteristics of the plant-life of a given region. Form, is the physical expression of the energy captured and transformed by plants, and it provides the basis for all ecological relationships. It is not surprising then that, broadly speaking, the plants of tropical regions that have access to the greatest input of radiant energy also have the greatest exuberance, while those of energy- and nutrient- limited environments, such as alpine moorlands and bogs, have a more restricted range of body plans. Inthecontinuumoftimethedanceofplantsisbothdevelopmen- tal and evolutionary. From this perspective the unity of all life can be seen in its infinite diversity. No longer can organisms be viewed in isolation but must be seen in the context of environment -- they are environment. The dancers are the plants and the music is their physicalandbioticrelationswiththeirenvironment.Theyaresimul- taneouslythecreatorsandthecreatedfortheythemselvescontribute to the music. As the orchestra of life tuned up, the first steps of sub-cellular andcellularstructureandphysiologywererehearsed.Initiallyitwas aslowdanceandthefirstnotesoftheevolutionoflifewerethesolar andthermalenergydrivingthechemistryofsimplelivingorganisms. The overture only hinted at what was to come and, for a long time, therewasasimplemelodywheretheprincipalplayerswerenotheard and the dancers were few, but even at an early stage the dance was one of innovation and improvisation. It was a dance of increasing sophistication accompanied by harmonies in a major key as plants viii PREFACE arose. They were the first truly terrestrial organisms and they trans- formed the landscape making it habitable for other organisms. Thedanceofplantsiscomplexbeyondourwildestdreams.Plants performepicdancesofcooperationandcompetition.Theydancewith theirenvironment,adaptinginstepwithitandmodifyingit,bycool- ingtheair,changingatmosphericcarbondioxideconcentration,pro- viding oxygen, making soil and by altering the relative abundance of the biotic components. They dance with each other in complex communities,exploitingwater,mineralnutrientsandsunlight,each finding a place to grow. They dance with other organisms, avoiding or repelling herbivores, attracting and feeding pollinators and dis- persersofseedsandfruits,andcooperatingwithfungitoexploitthe soil’s nutrients. There is an endless variation in the music and the dance, and the degree of complexity of their interrelationship. The growth of plants from seed is the source of some powerful metaphors for human life but mostly plants do not have immediate impact on us in terms of their adaptive evolution and developmen- tal processes. We appreciate them more for their beauty of form and colour, and grow them in our gardens and homes to lend harmony to our lives and as a reminder of wild nature. There may be more to‘phyto-psychology’thanwerealise.Humanshavehighlydeveloped sensesofcolourandspatialorderandtheremaybeaconnectionhere with our love of highly symmetrical plants such as cacti and succu- lents, or rosette plants such as African violets and primulas. Many bird-pollinated species such as fuchsias and columneas with their bright scarlet flowers, or herbs of the rainforest floor such as maran- tas with their strange metallic pigments, are perennial favourites in our homes. Plants lack the spontaneity of animals, whose movements, grace, complex behaviour, and often intricate and bizarre colours and pat- terns attract us in profound yet familiar ways. Animals arouse our curiosity.Theyarelikeusinsomanyways,yetaredifferent,andthis novelty requires investigation. Plants live in a different time dimen- sionandtelevisiondocumentariesoftenresorttotheuseoftime-lapse photographyinorderto‘animate’plants.Thisisperhapsunfortunate becauseitfailstoconveythetruenatureoftherelationshipbetween the spatial and temporal organisation of the plant world. Whileplantscouldalsobesaidtolackthe‘aloofness’thatissotan- talising about wild animals, we can easily touch plants and we can imagine that they pose for our photographs, but they still remain somewhat alien. Their texture is not that of the animal, although we can be intrigued when some leaf textures seem fur-like. Plants appear to lack movement or, if they do move, we are bemused. We know they are formed by the conversion of radiant energy, but the nature of their nutrition remains mysterious, and when they occa- sionallydevourinsectsweareamazed.Theyarelivingorganismsbut we cannot quite comprehend the nature of their experiences of the world, what it means to actually be a plant. Perhaps it is no great surprise that some of the earliest space invaders of science fiction were plant-like creatures, the triffids.