Ingrouille - Plants Evolution and Diversity (Cambridge, 2006) PDF
Ingrouille - Plants Evolution and Diversity (Cambridge, 2006) PDF
Ingrouille - Plants Evolution and Diversity (Cambridge, 2006) PDF
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 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
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Contents
Index 426
Preface
arose. They were the first truly terrestrial organisms and they trans-
formed the landscape making it habitable for other organisms.
The dance of plants is complex beyond our wildest dreams. Plants
perform epic dances of cooperation and competition. They dance with
their environment, adapting in step with it and modifying it, by cool-
ing the air, changing atmospheric carbon dioxide concentration, pro-
viding oxygen, making soil and by altering the relative abundance
of the biotic components. They dance with each other in complex
communities, exploiting water, mineral nutrients and sunlight, each
finding a place to grow. They dance with other organisms, avoiding
or repelling herbivores, attracting and feeding pollinators and dis-
persers of seeds and fruits, and cooperating with fungi to exploit the
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’ than we realise. Humans have highly developed
senses of colour and spatial order and there may be a connection here
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. They are like us in so many ways, yet are different, and this
novelty requires investigation. Plants live in a different time dimen-
sion and television documentaries often resort to the use of time-lapse
photography in order to ‘animate’ plants. This is perhaps unfortunate
because it fails to convey the true nature of the relationship between
the spatial and temporal organisation of the plant world.
While plants could also be said to lack the ‘aloofness’ that is so tan-
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-
sionally devour insects we are amazed. They are living organisms but
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.
PREFACE ix
. . . the train passes through a world of fancy, and you can look through the
misty panes at the green shadowy banks of grass and bracken. Here in their
season grow the blue agapanthus, the wild watsonia, and the red-hot poker, and
now and then it happens that one may glimpse an arum in a dell.
The writing of this book has taken much longer than we intended,
and many of our ideas have evolved in keeping with the progress of
the book. Inevitably this meant more changes. Originally, our plan
was to write a celebration of plant diversity as a successor to Diversity
and Evolution of Land Plants (Ingrouille, 1992). However, it soon became
obvious that there was a definite need for a new kind of approach, one
that would go beyond the bounds of conventional textbooks, of which
there are several excellent examples already available for students.
The research for such a book meant that the material we acquired
would fill several volumes, so painful decisions were made to cut the
ever-expanding prodigy down to an acceptable size. Meanwhile, other
events, including a lengthy research post overseas, intervened to delay
publication even further.
x PREFACE
Generally speaking, we believe that science and art are but two
ways of comprehending the world, two forms of creativity, and that
the scientific method, particularly in the realm of botany, could be
applied in a more phenomenological way, and even augmented by
intuitive approaches. Like art, science provides a way of knowing, of
making sense of the world, but the best scientists must go beyond
the scientific method. Current scientific procedures and methodolo-
gies are inadequate to explain much of the complexities of plantlife,
which often require subtle, broader-based holistic approaches. For
example, we have always been struck by the similarity of forms
throughout many unrelated plant families, be it at the level of gross
morphology or confined to the flower. Such phenomena are usually
explained away as instances of parallelism or convergence (or homo-
plasy, to use a currently popular term), and the explanation is always
framed in Darwinian terms of adaptation and natural selection. How-
ever, we feel that there is a deeper, underlying law of form or morpho-
genesis that constrains expression of form to within certain bound-
aries, and which cannot be understood simply in terms of linear cause
and effect. From a holistic perspective, the genome may also be por-
trayed as a self-organising network capable of producing new forms
of order. In addition, the aesthetic dimension has undoubtedly great
potential in promoting empathy for plants at the personal level as
well as a more widespread conservation ethic.
It is unfortunate that, in this age of instant information, general
botany and its long history are no longer taught, at least to the extent
that we would prefer. How we react to plants and how we ultimately
treat them is intimately bound up with our ways of regarding them.
Western science, at least since the time of Descartes and Bacon, has
promoted the idea that plants and other living organisms are objects
(res extensa) existing in isolation from the subject observer (res cogitans).
The disinterested objective method became the scientific method and
a cornerstone of the philosophy of science. We strongly believe that
this philosophy is flawed and has contributed to many of the difficul-
ties facing science today.
Thus, initially it may be difficult for some students to get situated
in this book, to see it in its entirety, for, at first sight, the combination
of different approaches is apparent. We make no apologies for this
PREFACE xi
because we do not reject the advances made in botany over the last
four hundred years. There is no doubt that reductionist science has
been singularly successful in elucidating much of our current knowl-
edge of plantlife, particularly relating to anatomy and physiology,
and in the fields of genetics, development and systematics. However,
in the age of the expert, plant science courses in universities are often
so narrowly specialised that we are in danger of losing sight of the
plants altogether, and therefore we feel that certain new approaches
or new perspectives are needed.
The traditional role of the amateur is the foundation upon which
botany was built. Without disparaging the importance of modern
computerised methods, and molecular and theoretical developments,
we encourage a return to a broad approach to botany that would re-
instate the importance of the amateur. Botany is an immense and
deeply satisfying subject and one that we can attest to providing a
lifetime of riches and rewards. It is therefore difficult for an under-
graduate to get the flavour of botany in three or four short years,
especially to develop a feeling for plants, and to understand the role
of plants in diverse ecosystems.
Where possible, we have tried to keep abreast of the multifari-
ous changes that have revolutionised so much of current biology in
recent years. Chapter 1 has been strongly influenced by developments
in complexity theory, including phenomena such as hypercycles and
autopoiesis (see Kauffman, 1993). It was felt necessary to touch on
such topics in order to give as complete a picture of the events lead-
ing to the early evolution of plant life, and for this reason we have
also included many aspects of the evolution and diversity of the algae,
although technically we would normally exclude them from the cate-
gory ‘plant’. There are several excellent and complementary texts on
the biology, evolution and diversity of the algae that we recommend.
In Chapter 2, although we have basically adopted a conventional
reductionist approach, we have tried to integrate this with some of
the most recent ideas in plant morphology and developmental genet-
ics, including the ‘theory of morphospace’. Much of this chapter was
influenced by the ‘process morphology’ of Rolf Sattler and his col-
leagues, although the philosophy behind this approach goes back to
A. N. Whitehead (see Whitehead, 1929), in addition to more recent the-
ories on developing and transforming dynamic systems and biological
form (Webster and Goodwin, 1996). There is no doubt that morphol-
ogy and developmental genetics has benefited from this trend away
from a static typology to a more dynamic process-orientated approach
but it has to be admitted that, by including the dimension of time,
practical difficulties in the analysis, interpretation, and description
of form are also introduced. This is particularly the case with respect
to descriptive morphology and the use of homology in classification.
There have been changes in the world of evolutionary botany over
the past 20 years. The familiar Neo-Darwinian paradigm is being aug-
mented by views that see evolutionary change as a result of life’s
inherent tendency to create novelty, and which may or may not be
xii PREFACE
first notes of life are the complex molecules and beating out with
the drum of metabolism. At first the noise is cacophonous as if the
orchestra is tuning up, but with the origin of cellular life, coordinated
metabolism arises, like snatches of melodies. Gradually at first, but
then more and more speedily, as the rhythms of cellular life assert
themselves, the first snatches of melody grow louder against the
cacophonous background. Simple melodies are taken up and repeated
in counterpoint as the seas and lakes become populated with living
organisms, some complex and multicellular. Later symbiotic associ-
ations between cells, like the origin of musical harmony, provide a
much broader potential for new life forms to diverge. The origin of
multicellularity and subsequently the functional specialisation of cell
types in the multicellular organism enrich the sound. At the margin
of land and water some of these themes were to be taken up and
elaborated by the first plants.
within the vesicle, for example, a polynucleotide analogue of RNA Life emerged, I suggest, not
could have been replicating within chemoton-like systems. simple, but complex and whole,
One key feature of the nucleic acids like RNA and DNA is their and has remained complex and
ability to splice together; parts of the molecule can be looped out whole ever since – not because of
or into the sequence of bases. The parts of the sequence excised are a mysterious élan vital, but thanks
called introns and those spliced together exons. Thus, in the evolution to the simple profound
transformation of dead molecules
of life before the emergence of bacteria, we envisage an ‘RNA world’
into an organization by which
where some molecules are active enzymes, others contain introns
each molecule’s formation is
and exons and convert themselves, either to RNA by self-splicing, or catalyzed by some other molecule
recombine to yield novel combinations by trans-splicing. Subsequently in the organization. The secret of
DNA took the replication and information-storing role, and proteins life, the wellspring of
the catalytic role, and RNA was left as an intermediary. In our ‘DNA reproduction, is not to be found
world’ proteins have taken over almost every catalytic activity. in the beauty of Watson–Crick
In a chemical system change is likely to extinguish a chemical reac- pairing, but in the achievement of
tion, but a living system has the potential to change without destroy- collective catalytic closure. So, in
another sense, life – complex,
ing the circular processes that makes its components. There is change
whole, emergent – is simple after
because self-replication is not perfect and slightly different but sta-
all, a natural outgrowth of the
ble daughter molecules are sometimes produced, but the living sys- world in which we live.
tem continues to replicate instead of spluttering to a halt. The system Stuart Kauffman, At Home in the
could evolve because some of these altered daughter molecules had an Universe, Oxford University Press
improved ability for autocatalysis as if they ‘remembered’ the changes 1995 pp. 47–48.
that brought them about. This was the birth of inheritance. With
the combination of self-regulating hypercycles and inheritance, the
brake was taken off chemical evolution and new kinds of metabolism
evolved.
Creativity, the generation of novelty, is a key property of all living
systems. A special form of creativity is the generation of diversity
through reproduction, from simple cell division to the highly complex
dance of sexual reproduction. Driven by the creativity inherent in
all living systems the life of the planet diversified in forms of ever-
increasing complexity.
1.2.1 Pigments
The portion of a pigment molecule that absorbs light and hence
imparts colour is called a chromophore. At the earliest stages it is
10 PROCESS, FORM AND PATTERN
Figure 1.13. Oxygenic photosynthesis. Simplified diagram showing the light reactions
of photosynthesis starting with the oxidation of water. Through the absorption of light in
Photosystem II the electrons gained from water are elevated to an excited state.
Subsequently they are transferred to Photosystem I. Here they are excited again by
absorption of light and transferred ultimately to NADPH. The action of Photosystems II
and I together is called non-cyclic photophosphorylation. The ATP and NADPH
produced as a result are input into the Calvin cycle. The dashed line shows cyclic
phosphorylation involving Photosystem I only and without the production of NADPH.
The diagram does not attempt to be chemically balanced. Not all the details are shown.
For example the cytochrome complex contains two cytochrome b and one cytochrome
f molecules as well as a Rieske iron–sulphur protein.
and produce sulphur in the same way as the sulphur bacteria. For
example the cyanobacterium Oscillatoria limnetica lives in sulphide-
rich saline ponds along with sulphur bacteria. Rather than giving
off oxygen, globules of sulphur accumulate on the outside of its
filaments.
1.3.4 Organelles
Organelles are intra-cellular structures that are either like mito-
chondria and chloroplasts, which are membrane bound, or centri-
oles, which are not. Mitochondria and chloroplasts have their own
genome, DNA in circular chromosomes like those of bacteria. Almost
all eukaryotes have mitochondria while plant cells also have plastids
including chloroplasts. A few eukaryotic organisms, the Archezoa,
lack mitochondria. This may be because they are truly primitive or
that they have lost mitochondria because of their peculiar lifestyle as
extra- or intra-cellular parasites. They also lack Golgi bodies or have
peculiar kinds.
24 PROCESS, FORM AND PATTERN
(a)
cyanobacteria. Other groups of photosynthetic protists have acquired
their plastids by secondary (or tertiary) endosymbiosis, with an
endosymbiont eukaryote already equipped with a chloroplast. For
example, in the photosynthetic euglenoids, three membranes sur-
round the photosynthetic organelles.
Cladoph r a
sper m
Life cycles
Three major kinds of life cycles can be distinguished; haplobiontic,
diplobiontic and haplodiplobiontic (Figure 1.23). Haplobiontic organ-
isms do not produce a diploid multicellular individual and produce
spores more or less directly from the zygote. Diplobiontic organisms
do not produce a multicellular haploid individual and have a haploid
stage restricted to the gametes. Haplodiplobiontic organisms alternate
32 PROCESS, FORM AND PATTERN
spores are produced in very large numbers. This is the case in the
brown alga Laminaria and most plants. However, the gametophyte is
large and the sporophyte is small in some organisms, such as the
brown alga Cutleria and most bryophyte plants.
The red algae (Rhodophyta) have an alternation of generations but
with three generations: two sporophytic ones and a gametophytic one!
The first sporophytic generation established following syngamy pro-
duces diploid carpospores, which germinate into a second sporophyte,
which produces haploid spores by meiosis.
The possession of an extended diploid phase in the life cycle, as
exhibited in organisms with a diplobiontic life cycle or haplodiplo-
biontic life cycle, has several important theoretical advantages over
the haploid condition. Syngamy between cells with homologous chro-
mosomes, but carrying different alleles, each coding for a product
with slightly different characteristics, creates a diploid that is het-
erozygous. In the diploid condition, if both alleles are expressed,
the individual may be better adapted to a wider range of conditions
because of its wider range of expression. In addition a range of differ-
ent alleles may be present in the population, with different individ-
uals having different combinations of alleles; the range of possible
genotypes, fitting a range of circumstances, is much greater than the
range of alleles. In each generation, random breeding and crossing-
over give rise to new combinations of alleles. This kind of genetic
variation between individuals provides the building blocks of evolu-
tionary divergence through natural selection.
In trying to understand the importance of sexual reproduction
and diploidy a reductionist approach focusing on individual genes
and alleles is unhelpful. Alleles are expressed in the individual along
with the alleles of many other genes, which can mutually alter each
other’s expression and selective advantage. It is the individual, not
the allele that is selected. In addition, the individual is not just the
sum of the activities of all its genes, its genotype. It is the external
form of the individual, the phenotype, that is selected, and this is the
product of an interaction between genotype and the environment in
its broadest sense. The advantage individual alleles confer to the indi-
vidual, in addition to being contingent on their genetic background,
is also dependent upon the individual’s history and present circum-
stance. The evolving species is a set of populations of individuals.
Species, populations, and individuals are each a trajectory in space
and time determined by interactions between their genotypes and
the environments they experience.
The importance of diploidy may be that it may provide a mecha-
nism to maintain high levels of genetic variation in sexual lineages.
In haploid individuals all alleles are expressed, exposing the resul-
tant characteristics to natural selection, and deleterious ones may
be eliminated relatively rapidly. However, in diploid individuals, if
an allele is recessive it is not expressed and is hidden from natural
selection, even if it is disadvantageous. It is only expressed when it
34 PROCESS, FORM AND PATTERN
(b) (d)
(e)
Along with the evidence of living chemical processes and the form of
cells, it is the presence of pattern that provides some of the earliest
evidence for living organisms. Fossil microbes from cherts and shales,
such as those from the Warrwoona Group from 3500--3300 million
years ago, are filamentous or colonial. Over many millions of years
greater complexity and diversity of organisms evolved. In the Gunflint
1.4 PATTERN: MULTICELLULARITY IN THE ALGAE 39
(d) (e)
(a)
(b)
new colony. In Scenedesmus the four cells are ornamented with spines.
In Eudorina, which can have 32, 64 or 128 cells, some posterior cells
are small and incapable of cell division. In some forms like Platydorina
there is a differentiation between the anterior and posterior part of
the colony. Volvox is the most complex free-floating colonial alga. It has
a single spherical layer of hundreds of cells, most of which are purely
vegetative, and others that divide to give rise to juvenile spheroids,
which are later released from the parent. These free-floating forms Figure 1.32. Hydrodictyon: (a)
exist in a fairly homogeneous environment, the only polarity being portion of net-like colony; (b)
the source of light, and consequently they show only weak differen- detail of net (a).
tiation, enabling them to orientate and swim towards light.
Table 1.4 The differences between the Chlorobionta and Streptobionta plus Embryobionta
Plants are actually very strange living creatures indeed. Their life is
alien to us. But this is their planet; they have made it and we live in
Figure 1.41. Thalloid their shadow. Plants seem static so that it is easy to forget that plants
chlorophyta in the Ulvophyceae. are living organisms. We associate movement with life. Though some
(a) Enteromorpha with a
plants look like pebbles (Lithops), they are not stones. If plants do not
unistratose tubular lamina; (b) Ulva
have life surging through them like animals, it trickles through them
with a bistratose flat sheet.
in a constant stream. Plants combine the stability of structure with
1.5 WHAT IS A PLANT? 49
Plants Animals
Autotrophic, photosynthetic Heterotrophic
Sessile Mobile
Indeterminate growth Determined growth
Modular construction Unitary construction with head and tail ends
No nervous system but symplasm Nervous system
Cellulose cell walls Cell walls absent or various
Vacuoles present Vacuoles absent
Sex cells arise late in development Sex cells separated from body cells early in development
their environment in any profound way. The sun baked the land and
the winds and rain scoured it. Soil development was minimal.
Plants have adapted to life on land by internalising the external
atmosphere and exploring the soil in an intimate way. Plants required
many adaptations in order to break away from the aquatic margins:
Hiscock, S. Field Key to the British Brown Seaweeds (England: Field Studies
Council, 1979).
Kauffman, S. A. The Origins of Order. Self-organization and Selection in Evolution
(Oxford: Oxford University Press, 1993).
Lee, R. E. Phycology, 3rd edition (Cambridge: Cambridge University Press,
1999).
Niklas, K. J. The Evolutionary Biology of Plants (Oxford: Oxford University Press,
1997).
Taiz, L. and Ziegler, E. Plant Physiology, 2nd edition (Sunderland, MA: Sinauer
Associates Inc., 1998).
Willis, K. J. and McElwain, J. C. The Evolution of Plants (Oxford: Oxford
University Press, 2002).
Chapter 2
Elongated cells packed with chloroplasts together form the pal- (a)
isade layer in the upper part of the leaf tissue. They are the most spe-
cialised photosynthetic cells in the plant. Below them, knobbly shaped
parenchyma cells form the spongy mesophyll tissue with many inter-
cellular spaces.
Collenchyma cells have a thickened primary cell wall. They may
vary from short and isodiametric to long and fibre-like. The cell wall
may be thickened at the angles of the cell or along one or more faces
of the cell. The cell wall in collenchyma is rich in pectic substances. It
is more organised than a parenchyma cell wall, with many layers of
fibrils. The fibrils are arranged in alternating layers in parallel, either
transversely or longitudinally. The cell wall is plastic, allowing the (b)
cell to deform without splitting or snapping and yet give strength to
the plant as it grows.
Parenchyma cells and collenchyma cells may make up tissues
called parenchyma or collenchyma, respectively. Parenchyma cells are
found in many other kinds of tissues and may be specialised in var-
ious ways to carry out different functions such as photosynthesis
or storage. Two important parenchymatous cells are the sieve tube
elements and companion cells of the phloem that function in the
translocation of nutrients. Collenchyma tends to be found only as a
strengthening tissue in a peripheral location in the plant, but similar
kinds of cells may be found elsewhere.
The other main cell type, sclerenchyma, has a secondary cell wall, Figure 2.4. Collenchyma:
which is produced inside the primary wall, after the cell has elon- (a) transverse; (b) longitudinal
section.
gated or enlarged. It makes the cell elastic, allowing it to deform, but
returning to its original shape after the stress is removed. The fibrils
are regularly arranged: in parallel to each other, mainly longitudinal
to the main axis, and in a weave with alternating layers at different
angles. The more acute the mean angle of the fibrils to the main
axis of the cell the greater the stiffness of the cell. However, if the
fibrils are orientated more transversely, the cell is less likely to break,
because the helically wound fibres can buckle inwards rather than
snap when put under strain.
The secondary wall is often produced unevenly in bands, rings,
helices or lamellae, conferring different characteristics to the cell; or
more continuously, and then it is pitted. The secondary cell wall does
not form over pits or primary pit fields but it sometimes arches over
the pit as a dome with an aperture at its apex. Coming in pairs in
adjacent cells these kinds of pits form a bordered pit pair. A tertiary
non-cellulose cell wall may also be produced in some cells.
Many sclerenchyma cells lack a protoplast at maturity. They form
a dead structural element in the plant and/or a conducting system in
the xylem tissue.
Two main kinds of water conducting elements are characterised
as tracheids and vessel elements, but, by looking at a range of plants,
it is clear that there is a complete spectrum of types from fibres, fibre-
Figure 2.5. Phloem: sieve cells
tracheids, and tracheids to vessel elements (Figure 2.6). Non-flowering
and companion cells.
seed plants have only tracheids but flowering plants generally have a
60 THE GENESIS OF FORM
(a)
(b)
Figure 2.7. Sclerenchyma: mixture of fibres and vessel elements in their xylem. So-called ‘non-
(a) transverse; (b) longitudinal vascular plants’ have analogous cells called hydroids. However, even
section.
those sclerenchyma cells that are dead at maturity and have ceased
to be conducting elements in the heartwood may have a prolonged
life before dying by becoming the receptacles of plant metabolites.
Sclerenchyma cells may be found in a specialised sclerenchyma
tissue but they are commonly found interspersed among other kinds
of cells in other tissues, as idioblasts. They may make up a large part
of the xylem. Sclerenchyma cells may be isodiametric (‘stone cells’ or
sclereids) or elongated fibres. Fibres can be very long, up to 10 cm
in hemp (Cannabis), and up to 55 cm in ramie (Boehmeria). They gain
this length by an extended period of growth after cell division. The
secondary wall is laid down after growth has ceased.
Plants utilise soil nutrients and light in minute diffuse amounts, are
rooted and relatively immobile organisms with rigid cells, and are
compelled to grow by cell division in localised, more or less perma-
nently embryonic regions called meristems. Those located distally in
the root and shoot apices, from which permanent tissue (the primary
plant body) is derived, are called apical meristems (Figure 2.11). There
are other meristems at leaf bases and margins, known as intercalary,
Figure 2.8. Secondary cell walls
marginal and plate meristems that function in the maturation and
and pitting.
shaping of mature leaves and reproductive organs, and in secondary
2.2 PLANT GROWTH AND DIFFERENTIATION 61
Meristems produce two kinds of daughter cells; those that extend leaf
and differentiate into specialised cell types and tissues such as epi- axilary
merist
dermis, cortex, vascular tissue, etc., and others which remain meris-
tematic. Cells differ from one another as a result of unequal divi- node
sion, differences in positional information, or both. The primary interod
epicotyl node
meristems are the sites of almost all apical growth, and the shoot
apex is carried upwards by differentiation and elongation of the pri- cotyledn
mary meristematic daughter cells. The developmental potential of adventious
hypoctl rot
particular cells is determined within the primary meristem itself
and not by cell signals from elsewhere, but the potential for growth
of the whole meristem is influenced by environmental factors such primary or lateral
tap rot rot
as light or moisture, in addition to correlative inhibition by other
organs.
rot
Assimilation of water and minerals occurs primarily at the distal apical
regions of root systems, while leaves, the principal organs of photo- merist
synthesis, are produced at the apices of shoot systems. The vascular
system that connects these processes must therefore develop simulta- Figure 2.11. Plant showing main
types of organ and location of
neously, resulting in a complex system of communication throughout
plant apical meristems.
the plant. This communication system is largely by means of plant
62 THE GENESIS OF FORM
(g)
(f)
(e)
(b)
(c)
(a)
(d) (h)
Figure 2.12. Vegetative growth substances although electrical phenomena are also involved.
regeneration: (a) corms
These growth substances are sometimes referred to as ‘hormones’,
(Crocosmia); (b) bulbils (Allium);
but this is not strictly accurate, and again reflects the zoocentric
(c) bulbils (Oxalis); (d) turions
(Hydrocharis); (e) stolons (Circaea); bias inherited in botany. Plant hormones include auxins, cytokinins,
(f) bulblets (Hyacinthoides); abscissic acid and gibberellins. They are described in more detail in
(g) viviparous plantlets (Festuca); Section 2.3. below.
(h) runners (Potentilla). The earliest studies of plant development relied on direct observa-
tions of shoot and root apices, and of microtome sections. With the
development of microscopy, especially scanning electron microscopy,
these techniques were considerably enhanced, but the problem of
integrated development and the actual genesis of form remained
elusive.
An understanding of the role of meristems and the processes
involved in tissue and organ formation is crucial for a deep appre-
ciation of plant development and ultimately its place in plant evolu-
tion. It is important for the student to develop a dynamic view of the
plant world, both in terms of the morphological potential that plants
possess, and the way this potential expresses itself through ontogeny
and phylogeny. The following account largely describes the processes
that take place in the mature plant.
an axillary flower or as a lateral shoot. Each single leaf and its axil-
lary bud, plus a portion of the shoot immediately below it, can be
conceived of as a unit or metamer, and the timing between the pro-
duction of each successive metamer in the meristem has been termed
a plastochron.
Zonation of the meristematic region appears to be widespread in
Figure 2.15. Apical meristems
seed plants although the specific characteristics of the zones are var-
showing leaf primordia: (a) Elodea;
ied. These zones function with a high degree of independence in the
(b) more typical flowering plant.
generation of shoot tissues although the capacity to regenerate entire
apices is present in both central and peripheral zones. Based on cell
structure and growth rate, two main zones with separate complemen-
tary functions may be delimited, the promeristem near the apex tip
and the primary meristem below this.
Shoot apical meristems are radial or elliptical in shape and range
greatly in size. The largest are found in pachycauls such as cycads
and palms. Generally, the size of the promeristem and the apical
meristem as a whole remains constant for a species, but there is
usually some degree of relationship between meristem size and plant
vigour. Shoot apical meristems have characteristic cells, which are
almost isodiametric, small and thin-walled with dense cytoplasm and
no conspicuous vacuole. The promeristem includes the apical initial
cells and their most recent derivatives that have not yet undergone
any of the changes associated with tissue differentiation. Apical initial
cells are the source of meristematic cells, and retain their potential
for continued division. At least one product of each division stays in
the meristematic region.
In whiskferns (Psilotum), clubmosses (Lycopodium), horsetails (Equi-
setum), some ferns (e.g. Dryopteris), and in bryophytes, a single apical
initial cell, shaped like an inverted tetrahedron or pyramid, may be
recognised (Figure 2.14). It divides sequentially, producing daughter
64 THE GENESIS OF FORM
cells from each of its lower sides. There is however, considerable vari-
ation in the apical zonation of gymnosperms and ferns.
The patterns of cell divisions in apices of seed plants are less reg-
ular and do not define any unique locations for initial cells. All cell
lineages can theoretically be traced back to single apical cells, the
founder cells, but in most seed plants no specialised apical initial cells
can be found. In experiments with chimeras, plants constructed by
grafting two genetically distinct tissues together, there can be more
than one initial cell. Relatively exact determination of the fate of
developing cells is uncommon but there are some known examples.
The flower primordium in Arabidopsis is probably initiated from four
cells derived from the longitudinal division of two apical initials, but
this may be a special case since Arabidopsis is a member of the Bras-
sicaceae, a family also called the Cruciferae, a name that refers to its
cross-shaped flowers with parts produced in twos and fours.
It is the relatively inactive promeristematic region that is the ulti-
mate source of new tissues and overall patterning of organs even
though the region itself forms few cells and pattern formation occurs
before the primary meristem stage. In Buvat’s theory the ‘méristème
d’attente’, a central zone of hardly dividing cells is essentially passive,
and it is the outer ‘anneau initial’ that generates new cells. However,
during reproductive development, the cells of the méristème d’attente
are activated and participate in the formation of inflorescences and
flowers. The reproductive organs of lower plants do not conform to
this pattern of development but may arise from any actively divid-
ing meristematic tissue, often from marginal regions of the apex;
for example, the leptosporangia of ferns may arise from superficial
protodermal cells.
Promeristem cells are not clearly differentiated from one another.
They are neither clearly polar nor do the microtubules at the tip of
the promeristematic dome have consistent orientation. Nevertheless,
differentiation occurs, in which at least four cellular types are recog-
nisable by the time the primary meristem stage is reached. By then,
cell divisions and cellular sizes increase, often rapidly. Cell divisions
in the promeristems of shoots do have characteristic orientation, and,
together with cell size, stainability, and internal architecture, have
allowed the recognition of subzones, although these vary widely.
In ferns the outer layer is very obvious because the cells are elon-
gated anticlinally, perpendicular to the surface. Commonly, in the
flowering plants, an outer layer(s) of cells of the promeristem, called
the tunica, and an inner mass of cells, called the corpus, are dis-
tinguished. The tunica comprises one to five (usually two) superficial
layers of the apex above the level of the youngest leaf primordium,
in which usually only anticlinal divisions occur. In the monocots and
gymnosperms some periclinal divisions have been observed whereas,
in the inner layers, cell divisions are in many different directions. In
gymnosperms such as Pinus an apical zonation has been described
where there is a group of slightly larger apical initials that have a
low affinity for cell stains. They give rise to a group of central mother
2.2 PLANT GROWTH AND DIFFERENTIATION 65
cells from which regular files of small vacuolated cells, called rib
meristems, arise.
The tunica and corpus do show some biochemical differences
between their component cells and the quantitative distribution of
cellular organelles, both of which may be important for cell lineages
but not for the organisation of the promeristem itself. Although the
actual number of cell layers in the tunica is variable, usually two or
more outermost layers of the apical dome are consistently at right
angles to the surface and have the exclusive function of forming the
protoderm and ultimately the epidermis. The other tissues formed
by the promeristem are a ground meristem which matures primar-
ily into various types of parenchyma such as cortex and pith and a
procambium, normally produced in strands, from which the future
primary vascular tissues are formed. In the stem each procambial
strand becomes a vascular bundle.
Xylem cells are formed in the procambium in two phases
(Figure 2.16). The protoxylem is produced while the organ is still elon-
gating. Protoxylem cells are thickened by annular rings or helices of
secondary cell walls, which allow the cells to stretch. There is a grad-
ual transition to metaxylem cells that differentiate after the organ
has elongated. Metaxylem cells have a wider diameter and have wide
66 THE GENESIS OF FORM
2.2.3 Branching
Much of the character of a plant body is determined by branching pat-
tern. A stem may be thought of as a succession of internodes, while
the combination of a leaf with its node and underlying internode
represents a basic structural unit of plant architecture that allows
the description of plant development regardless of the degree of
complexity. These modules are sometimes referred to as ‘phytons’ or
‘phytomers’, and will be discussed more fully in Chapter 3.
During ontogeny these modules are repeated to reveal several lev-
els of organisation that are really different stages of a common pro-
cess of growth and transformation. The whole flowering plant may
not only be regarded as a module, but also a branching axis or even
a single branch may be a module. One way of defining modules is
68 THE GENESIS OF FORM
that they each represent the growth of a plant ending in the pro-
duction of a reproductive organ, either an inflorescence or another
structure.
The concept of the ‘module’ was defined by Prévost as a ‘leafy axis
in which the entire sequence of differentiation is carried out from
the initiation of the meristem that builds up the axis to the sex-
ual differentiation of its apex’. In this terminology modules are then
themselves made up of repeat units called metamers. Therefore, each
metamer of the vegetative axis is the leaf, plus its place of attachment
Figure 2.18. Orthotropic axes
grow in three dimensions.
to the stem, and in the angle between the base of leaf and stem an
axillary bud, together called a node, and the portion of stem between
the node and the adjacent node called the internode.
(a)
One metamer is added to another, as the plant grows to form
a stem or branch. It is possible to derive a great diversity of shoot
systems from a number of simple rules for the timing of the pro-
(b)
duction, development and rate of extension of the basic leaf--stem
metamer, and the subsequent development of the axillary buds. Sim-
(c1) ilar metamers may behave slightly differently becoming either a
(c2) vertical or horizontal axes. A vertical axis, which is also called an
orthotropic axis, has an essentially radial symmetry. The horizontal,
(d1) or plagiotropic axis, is normally dorsiventrally flattened but can arise
in other ways. A plant may have only one of these kinds of axes, or
both. In a few species, a branch may start growing orthotropically and
(d2)
finish plagiotropically or vice versa. In addition branches may orien-
tate themselves as they grow, either more actively, as in procumbent
(e1) plants, or passively, as in decumbent plants.
Some plants have an unbranched axis. In branched species lateral
(e2) branches may arise in different places, for example, either at the base
or distally. Alternatively, they may be produced continuously along
an axis, or rhythmically. A few plants have short-lived branches that
Figure 2.19. Plagiotropic axes behave like compound leaves. In the bryophytes branches arise below
often grow in two dimensions and
the leaves and not in the axils of the leaves.
can be of several types: (a)
The simplest kind of branching arises by the division of the api-
distichous arrangement with leaves
in the same plane; (b) anisophyllous cal meristem into two equal halves. This kind of branching, called
with leaves of different sizes; dichotomous, was the earliest to evolve and can be observed in fossils
(c) simple plagiotropic growth; such as Cooksonia of the Late Silurian, and in Early Devonian plants
(d) plagiotropism by apposition; such as Rhynia. It can also be observed in living plants such as the
and (e) plagiotropism by whiskfern Psilotum and lycopods, an even in some relatively specialised
substitution. plants such as palms, cycads and pandans, although frequently in
these cases it has arisen not by true dichotomy of the apex but by
an abortion of the apex and the growth of two lateral buds, and is
hence called pseudo-dichotomous branching. In plants with sympo-
dial growth each shoot apical meristem has a limited lifespan. The
(a) (b)
axillary bud nearest to the apex then takes the place of the apical
bud, giving the shoot a characteristic zigzag appearance. The apical
bud may be aborted or become determined as a reproductive organ.
Figure 2.20. Orientation of Even in the Early Devonian some plants show a greater domi-
branches: (a) procumbent;
nance of one of the dichotomising axes, as in Asteroxylon, illustrating
(b) decumbent.
a tendency towards the normal pattern most frequently seen today,
2.2 PLANT GROWTH AND DIFFERENTIATION 69
i.e. axilliary branching in which a dominant main stem with its apical
meristem gives rise to weaker lateral branches. The arrangement of
lateral branches follows that of the leaves since branches arise from
axillary buds at the base of each leaf. This evolutionary transition
from dichotomous branching to axillary branching is the manifesta-
tion of the greater integration of growth of the plant, from one in
which different apices of the plant behave entirely individually, to
one in which there is coordinated growth of different parts of the
plant.
Branches may be produced immediately so that growth is contin-
uous, a process called syllepsis. This occurs in herbaceous plants and
many tropical trees. In most temperate trees, however, the bud meris-
tems have a period of dormancy before producing a branch, so that Figure 2.21. Dichotomous
branching in the Devonian plant
growth is rhythmic, a process called prolepsis. The difference between
Rhynia.
a sylleptic and a proleptic branch can be recognised because, in the
former, the basal internode is elongated and, in the latter, there may
be many very short basal internodes sometimes marked by bud scales
or scars. Rhythmic growth can also be recognised by regular changes
in leaf size and by the formation of growth rings in the wood.
(a)
layers comparable to the tunica and corpus. Root meristems are dis-
rot tinguished by a quiescent centre at the tip that is characterised by
hair
z one little or no DNA synthesis or mitotic division, and which therefore
(b) may not grow at all. There is a root cap ahead of the root apex, with its
own meristem, in the region known as the calyptrogen. The meris-
tematic cells of the root apex therefore produce cells that mature
z neo of
both acropetally and basipetally. The root cap meristem may become
elongation isolated from the apical meristem by the quiescent centre. In this case
the meristems are said to be closed. In other cases the root cap meris-
z one of
cel tem may produce cells that become part of the epidermis or cortex
divson (c) of the root proper. It seems that one kind of root apical meristem
may be converted into the other by small variations in their relative
Figure 2.25. The primary root: activity. The root cap protects the apical meristem proper as the root
(a) general view showing root cap, pushes through the soil. Cells from the root cap slough off as the
elongation zone and root hair root advances through the soil aided by lubricating mucilage that
zone; (b) detail of root hairs; encourages a microflora in the rhizosphere. Much of the growth in
(c) detail of root cap. roots occurs in the sub-apical region and the files of gradually matur-
ing cells that make up this region can be traced to the sub-terminal
region immediately below the root cap.
Initially roots are fine and delicate. The root apex is much smaller
than that of the stem, generally about 0.2 mm in diameter, allowing
it to penetrate most soil spaces. The small diameter of the root also
increases the surface area available for uptake relative to the volume
of the root but they do not absorb over their whole surface. Root hairs
increase the surface area even further and absorption is concentrated
in the root hair zone.
Some species may produce roots of two different sorts; long
roots of unlimited growth and short determinate roots. Three cat-
egories of root systems have been identified based on the distribu-
Figure 2.26. Anatomy of root tion of root diameter classes and the degree of development of root
meristem. hairs: graminoid root systems are fine and delicate with profuse root
hairs, resulting in a very high absorptive area to root volume ratio;
2.2 PLANT GROWTH AND DIFFERENTIATION 71
(a) more rapidly it is likely to continue developing and the larger are its
effects on the rest of the plant.
The initiation of new organs is due largely to the interaction of
roots and shoots but these interact in different ways to produce basal
or apical branching in different plants. These have complementary
rather than identical effects on vascular differentiation. Developing
shoots enhance root development, and vice versa. Although roots and
shoots have continuous reciprocal effect on one another through-
out development, they can compete with each other for metabolites.
In contrast, signals received from the rest of the plant may merely
limit the initiation of shoots and roots. The movement of substances
(b) towards the region in which they are used for growth serves as a
signal of inhibition.
Expanding tissues, the ones with the largest influence, are the
major sites of new organ synthesis. They may also be the sources of
growth factor signals that are responsible both for inhibition, and
for the development of the apex. The apex is the source of the origi-
nal inductive signal, and the supply of limiting growth factors to an
apex would be a function of its ability to enhance the development
of complementary organs while simultaneously inhibiting competing
ones. Thus, an apex polarises the axial tissues leading to a diversion
of supplies towards the dominant apices. Such apical signals orien-
Figure 2.35. Branching pattern:
(a) basal (basitony); (b) apical tate differentiation in accordance with the axis of their movement
(acrotony) branching. through the plant thereby inducing complementary initiation where
they accumulate.
Roots are the main sinks for auxins, resulting in the differenti-
ation of vascular tissues along the axis from the developing tissues
of the shoots to the roots. Roots, however, are also active sources
of growth factor or other signals, and developing root tissues will
orientate differentiation towards themselves. New organs dominate
the plant and orientate tissue differentiation towards themselves.
Apical parts of the shoot inhibit or dominate the growth of lat-
eral buds, a phenomenon known as apical dominance. Such relations
obviously influence the form of a plant, but there are variations in
the sensitivities of subordinate tissues so that some plants branch
mainly basally and others more apically. Laterals differentiate in the
same way because of the presence of the same dominant organ, for
example lateral shoots are frequently plagiotropic (e.g. Araucaria). The
traits assumed by lateral branches (e.g. dorsiventrality) are often more
extreme and less readily changed (more determined) than mere direc-
tion of growth.
There are a variety of structural gradients in plants owing to dif-
ferent developmental potentialities, such as differences in age along
the axis. A gradient of the capacity to form roots could result in the
first roots being initiated, preventing further root development and
initiation. Inhibition and initiation of development are also exerted
by other plant organs. Lateral buds that have started growing inhibit
the development of the main shoot and rapidly growing leaves inhibit
buds and induce root initiation.
2.3 THE INTEGRATION OF DEVELOPMENTAL PROCESSES 77
(a)
2.3.3 Electrical signalling in plants
Plants do not have a nervous system but it is not quite true to say
that only in science fiction do plants move. When touched, a wave of
movement passes over the sensitive plant (Mimosa pudica) as it closes
its leaves (Figure 2.38). Cassia nictitans, and species of the aquatic herb
Neptunia, also have sensitive leaflets. Sensitive stamens are relatively
(b) widespread and are found in Centaurea and Berberis (Figure 2.39) for
example, and have achieved a high level of development in the trigger-
plants (Stylidiaceae). The carnivorous plants such as Venus’ fly-trap
(Dionaea muscipula) and the bladderworts (Utricularia spp.) respond very
rapidly to the touch of their prey. In Utricularia, when the catch on
the trapdoor is sprung, the lid of its bladder flips open and its prey
is sucked inside to be digested. The suddenness of the response is
Figure 2.39. Sensitive stamens brought about by an electrical signal, an action potential analogous
of Berberis react to the touch of a
to that of an animal nerve cell that passes along parenchymatous
pollinator.
cells linked by plasmodesmata. The signal causes sudden changes in
the permeability of the plasmalemma of the target cells. Water floods
out and the hinge cells change shape in Utricularia, active excretion
of water from the bladder resets the trap. In Mimosa pudica, special
pulvinus cells at the base of the leaflets rapidly lose turgor, so making
the leaf close.
There is also a broad range of slow plant movements, tropisms,
which can be revealed by time-lapse photography. Some movements
are more or less reversible. These are mediated by changes in turgor,
although less explosively than the ones described above. There are
heliotropic responses, orientating flowers or leaves to sunlight, or
opening and closing of flowers, especially at dawn and dusk.
These reversible changes are not the main way in which plants
‘behave’. From our zoocentric point of view it is easy to forget that
2.3 CELLULAR DETERMINATION 81
The finest veins make up by far the greatest part of total vein
length, for example 95% in Amaranthus. Areoles may be very simple,
consisting of only a few tracheids. The xylem is primary xylem
because the finest veins are produced while the lamina is expand-
ing, so the tracheids have to be able to stretch. Phloem may also be
present but sometimes it is only present in the previous order of
veins closer to the midrib. The vein may be surrounded by an obvious
sheath of sclerenchyma or parenchyma cells. Transfer cells are found
as a sheath surrounding the phloem. They are companion cells or
specialised parenchyma cells.
With dichotomous venation the water diffusion pathway to the
mesophyll and palisade cells is long because the veins are often quite
far apart. In the cycads and conifers, however, this is compensated by
the presence of a transfusion tissue surrounding the vascular bun-
dles. Short, wide, nearly isodiametric tracheids are arranged radially
around the bundle. In the cycads there are two transfusion tissues,
one between the vascular bundle and the endodermis and another
between the spongy mesophyll and the palisade parenchyma.
Most monocots and some dicots have parallel venation. The veins
run longitudinally down the leaf connected by thin commissural bun-
dles. Alternatively there is a midrib from which veins run out laterally
in parallel. The arrangement is related to the way the leaf expands,
either longitudinally or laterally. In those with longitudinal venation,
there is a basal intercalary meristem. The potential for unlimited
(i.e. indeterminate) growth by the activity of this meristem is limited
because of the problem of conducting water into the lamina across
this relatively immature region. In plants such as Yucca, the leaves
are so slow growing that cells start to differentiate within parts of
the meristematic region, thereby maintaining a vascular connection.
Nevertheless even in these species the potential for leaf extension
from the base is limited to very young leaves.
The differences between the parallel venation of monocots and
the reticulate venation of dicot leaves has led some workers to sug-
gest that monocot leaves are derived from the petiole, or petiole plus
midrib, of the dicot leaf. Leaves of this sort are known from other
groups, where they are called phyllodes.
Internally the leaf is highly differentiated with an upper palisade
layer and a lower spongy mesophyll (Figure 2.44). Support of leaf tis-
sues, mainly conferred by the turgor of the cells, is enhanced by
localised regions of collenchyma or sclerenchyma, especially as bun-
dle sheaths around the vascular bundles. The bundle sheath may
extend as a girder to reach either one or both epidermises. Non-
vascular fibre bundles may also be present. Often the margins of the
leaf are strengthened by the presence of sclerenchyma and a thick
Figure 2.43. Epidermal cells:
epidermis.
various stomatal subsidiary cell Usually the epidermis is different on the upper or adaxial surface
arrangements. from the lower or abaxial surface. The lower surface usually has stom-
ata. Sometimes these are protected by being sunken in chambers,
2.4 CELLULAR DETERMINATION 85
outer whorl. Sepal primordia arise first, in the outer whorl around
the periphery of the meristem, then petals, then stamens and finally
the gynoecia.
The idea that organisms develop epigenetically dates back to Cas-
par Friedrich Wolff in the late eighteenth century, although it was
Johann Wolfgang Goethe who really elaborated the idea that floral
organs and leaves are merely different manifestations of a common
underlying theme. Through the study of developmental ‘abnormali- (a) Normal
ties’ such as peloric flowers, Goethe was able to demonstrate that the monosymmetric flower
organs of staminate whorls were capable of developing in a manner
similar to the organs of the petaloid whorls. In many cultivated flow-
ers, fuller double flowers have been produced by manipulating the
expression of organ identity. This phenomenon was coined ‘homeo-
sis’ by Bateson in 1894. There is a transition between organs in some
species such as that between petals and stamens in Nymphaea.
The discovery of homeotic organ identity genes controlling the
expression of repeating morphological units has accelerated the study
of floral morphogenesis. Within plants these homeotic genes are (b) Mutant peloric flower
called MADS-box genes. Changes in the regulation of these genes
Figure 2.51. Antirrhinum
may have contributed to the establishment and structural evolution
flowers.
of flowers. The homeotic genes have arisen by duplication and have
the same basic identity. The MADS-box is a highly conserved sequence
motif found in a family of transcription factors. It codes for part of
the master protein (the homeobox domain) that makes direct contact
with the DNA at the binding site. The conserved domain was recog-
nised after the first four members of the family, which were MCM1,
AGAMOUS (AG), DEFICIENS (DEF) and SRF (serum response factor), and
the name MADS (M) was constructed from the initials of these four
‘founders’. Most MADS-box domain factors play important roles in
developmental processes and have been called the ‘molecular archi-
tects’ of flower morphogenesis. A rough reconstruction of the history
of MADS-box genes has already been made. These monstrosities are so to speak,
Similarities in the base sequences of MADS-box genes suggests that the experiments that nature made
these genes have evolved over millenia through the process of gene for the benefit of the observer: there
duplication, by the building of one set of events on another. This we see what organs are, when they
has allowed a reconstruction of land plant phylogeny based on such are not joined together; there we
sequences. The last common ancestor of plants, animals and fungi recognize what they really are, when
an accidental case has prevented
that existed about one billion years ago had at least one MADS-box
them from enlarging. A. P. de
gene. In the lineage leading to green plants, the MADS-box (M) is fol-
Candolle, Organographie végétale
lowed by homologous genes which have been termed the IKC region. (Paris: A. Bellin, 1827).
The last common ancestor of ferns and seed plants that existed
about 400 million years ago already had at least two different genes
of the MIKC type. Large numbers of gene duplication events have
produced a diversity of MADS-box genes in ferns (CRM type) that
diverged very early on from seed plants. The common ancestor of gym-
nosperms, Gnetales and angiosperms, which existed about 300 mil-
lion years ago, already possessed at least six different MADS-box genes
that are present in living angiosperms (Figure 2.52). The ancestors of
the angiosperms as we know them today possessed all the gene lin-
eages from which the floral homeotic genes have evolved.
92 THE GENESIS OF FORM
the waves, organisms dance restlessly across its surface. But then why
do certain forms arise again and again?
Goodwin believes that the processes that alter the shape of Acetab-
ularia during morphogenesis are those very processes that create
generic forms in the organismic world. Despite the possibility for
almost limitless forms, they explain the predominance of generic
forms or archetypes over a limitless number of ‘possible worlds’. This
is because these structures are highly probable and arise from the
dynamic processes of morphogenesis. Goodwin’s theory is especially
consistent with field models in which patterns are initially described
by a set of harmonic functions (linear forms), but as pattern devel-
ops, the nonlinear features are expressed and distinctive wave-shapes
emerge, as stable forms. A crucial aspect of this theory is that the
parametric values in the equations describing the field are deter-
mined not just by environmental factors but also by genetic deter-
minants that are the result of the previous evolutionary history of
the organism. There may be some congruence between the Theory
of Morphospace and the Morphogenetic Field Theory of Sheldrake,
but more research is required to elucidate so many aspects of how
organismal development proceeds and how the wondrous diversity of
form in the living world is achieved.
Endless forms?
(a)
Relative absorption (b) (c)
protein
at all. These differences allows the root system to explore the soil
more thoroughly. Roots grow downwards (positive gravitropism) and
stems upwards (negative gravitropism) in response to gravity. Vertical
growth is called orthogravitropism, whereas, branches, petioles, and
rhizomes are more horizontal and display diagravitropism. Plant
organs with no response to gravity are called agravitropic. Gravity is
perceived by plastids, especially amyloplasts, in the cells of the root
cap.
LONG-DAY PLANT
Gravity and wind constrain the height to which plants can grow,
but they cannot make plants that are genetically ‘programmed’ to
be small any taller. Other environmental factors such as daylength
and temperature, and biotic influences may have direct or indirect
effects on development, flowering times, etc., but adaptations to
such processes alone do not establish the overall construction of
plants.
Before the development of genetics and modern microscopy, the
dominant view of development was that of the preformationists who
believed that a tiny version of a human being was encapsulated in
a sperm cell, and developed in the mother’s womb until birth, the
mother providing nutrition only for the developing foetus. Accord-
ing to Lewontin, modern developmental biology is a version of the
preformationist idea in disguise, i.e. genes determine the final form,
while the environment is merely the platform for gene expression
and organismic sustenance.
3.2 THE NATURE OF EVOLUTIONARY PROCESSES 105
These theories have remained marginal to orthodox Neo-Darwinism, Two quotations from chapter five
which is essentially a mechanistic explanation for organic evolution. of On the Origin of Species (1859):
What is frequently overlooked is that this only constitutes part of
I know of no case better adapted to
Darwin’s theory of evolution. Many biologists rightly feel that there show the importance of the laws of
is something incomplete about simple mechanistic explanations. correlation in modifying important
A frame of reference for developmental biology of only genes and structures, independently of utility
cell organelles, while environment is merely a background factor, is and, therefore, of natural selection,
clearly inadequate for the total developmental epigenesis of plants. than that of the difference between
Development is a transformational theory of change whereas current the outer and inner flowers in some
evolutionary theory is a variational theory of change. What is long Compositous and Umbelliferous
overdue is an integration of both theories in a holistic or systems plants.
approach that emphasises the way organisms function as intercon- . . . we see that modifications of
nected wholes. In recent decades there has been a re-awakening of structure, viewed by systematists as
of high value, may be wholly due to
generative or structuralist aspects of plant development.
unknown laws of correlated growth,
and without being, as far as we can
see, of the slightest service to the
3.2.3 The dance through morphospace species.
The historical emergence of different forms may be more fully under-
stood in the context of a ‘theory of morphospace’ such as that
described by Goodwin. As Stephen Jay Gould says of evolution, ‘it has
no purpose, no progress, no sense of direction. It’s a dance through
morphospace, the space of the forms of organisms’. This approach
provides botany with a logical, dynamic foundation and somewhat
reduces the role of history as an explanation of plant form. The ‘new’
biology is a science of complex systems concerned with dynamics
and emergent order. Viewed in this way, all the old biology changes.
Instead of the tired metaphors of conflict, competition, selfish genes,
climbing peaks in fitness landscapes, what you get is the metaphor
of evolution as a dance, and it is the rules of the dance that is the
subject of evolutionary biology.
Individuals of a plant species can be thought of as constituting
a dynamic evolving system interacting with an environment that is
simultaneously heterogeneous and dynamic. The net result is that
the course of evolution can proceed along highly diverse pathways.
Without a dynamic changing Earth there would be no major organ-
ismic diversity. Therefore, the successful study of plant form ideally
should be within a four-dimensional ecological framework involving
the interaction of plant, environment and time. This is a systems
theory of plant evolution, i.e. the evolutionary dynamics of plants
are determined by the structural organisation of the genome and
the epigenetic system, and embracing mechanisms of change such
as mutation, recombination, random drift and selection. It must also
stress the cohesion of the genotype and the integration of the devel-
opmental system. However, it goes beyond orthodox interpretations,
which regard organism--environmental interactions as theoretically
reversible. Under a systems model of plant evolution, change is irre-
versible since it is essentially correlative, and the outcome destroys
the conditions that made such evolutionary changes possible in the
first place.
108 ENDLESS FORMS?
(a)
The expression of a particular genotype in a particular environ-
ment is called the phenotype. Deterministic factors ultimately have a
genetic basis, and are responsible for the conformation to the phys-
iological and morphological parameters of the species. Nevertheless,
environmental or opportunistic factors impinge on plant form and
the ecological requirements of a species. Both factors combine to
give a historical trajectory to a species (heredity). It is from the rel-
ative contributions of these contrasted processes (genotype and phe-
notype), and their interaction with the environment that plant form
emerges. The way plants develop varies widely and, in the majority
of species, there is a norm of reaction, i.e. there is a spectrum of pos-
sible outcomes. Ability to respond to chance environmental variables
is ultimately determined by genotype, and differs widely in different
groups of plants, in closely related species, and even between individ-
uals of the same species. Such responses also vary at different times
(b) in the life cycle. In some species with more precise growth, develop-
ment appears to be more deterministic; for example certain palms
and arborescent monocots usually cannot respond to crown damage
because they lack lateral meristems. Predictability of vegetative form
can be shown to be widespread in non-flowering plants from lycopods
to conifers. In other groups of plants, predictability of final form is
more elusive. This stochastic response is usually expressed by reit-
erative vegetative growth and is one of its most important adaptive
features of plants, but it can only be assessed after the initial deter-
ministic component of growth has been recognised. Thus, it may be
impossible to predict how any individual plant will develop in a given
environment.
In marked contrast to vegetative parts, floral and fruit morphology
are highly deterministic, with little scope for opportunistic develop-
ment, which is one reason why these structures have lent themselves
Figure 3.17. Predictable to a typological classification, and are so important for plant system-
architectural forms in atics. Naturally, there are differing views as to the extent to which
non-flowering plants that follow a plant form is determined by their genes or by chance events produced
determinate pattern of growth: (a) by the interaction of the genotype with the environment.
lycopod; (b) Araucaria heterophylla.
was convinced that not only were there manifold effects of single
genes (pleiotropy), but that systems of interacting genes (epistasis)
were pervasive. He believed these interactions were context depen-
dent. Unfortunately, it was within the context of other genes present
rather than these plus an ecological context as well. Adaptive evo-
lution in Wright’s view is local, rather than global, and that the
fitness landscape permits multiple peaks of various heights. It was
his Shifting Balance Theory that allowed phenotypes to move from
local optima.
are particularly diverse. Leaves vary in size from tiny scales a few
millimetres in size to the huge compound leaves of some palms and
ferns. Plant morphology, including
Compound leaves are divided pinnately or palmately into leaflets morphogenesis, remains relevant to
or segments. The segments of a pinnate leaf (pinnae) may be fur- practically all disciplines of plant
ther divided (into pinnules) and subdivided up to five times. The biology such as molecular genetics,
midrib of a compound leaf is called the rachis. Each segment of physiology, ecology, evolutionary
biology and systematics . . . Most
a compound leaf arises from a separate primordium. This can be
commonly, morphology is equated
seen very clearly in the unfolding fern frond with its tightly packed
with classical morphology and its
primordia, in the fern crozier. Some plants have pseudo-compound conceptual framework . . . plants . . .
leaves where leaf segments arise by the splitting along predetermined are reduced to the mutually
lines of weakness of a single lamina. Pseudo-compound leaves are exclusive categories of root, stem
found in banana, palms, and the ubiquitous houseplant Monstera for (caulome) and leaf (phyllome). This
example. Compound leaves maximise the photosynthetic area while ignores the fact that plant
releasing the potential mechanical strains a single surface would suf- morphology has undergone
fer. Anisophylly may be present with the leaves held in a lateral fundamental conceptual, theoretical
and philosophical innovation in
position are larger than those that are either above or below the
recent times . . . If, for example,
shoot.
plant diversity and evolution are
As with the classical model of shoot architecture, study of early seen as a dynamic continuum, then
plants in the fossil record challenges our preconceptions of the nature compound leaves can be seen as
of leaves. The earliest plants were leafless. It is clear that leaves have intermediate between simple leaves
originated in several ways. Bower suggested that they evolved as ena- and whole shoots. Recent results in
tions from spines that became vascularised. molecular genetics support this view.
The telome theory of Zimmermann suggests microphylls might From R. Sattler and R. Rutishauser,
have evolved by reduction of a non-fertile lateral branch system, and 1997
like leaves but are actually modified stems or branch system. The
degree of resemblance to true leaves varies, and can be remarkably
close.
In some cases, as in Phyllonoma and Ruscus, it is difficult to be sure
about the nature of the ‘leaf’ until it produces a flower or fruit on
its margin or surface, something a true leaf never does. But what
is a true leaf? Leaves are very diverse in structure and development.
Fern fronds are leaves that bear the reproductive sporangia. They have
been described as megaphylls and are not considered homologous to
the leaves of bryophytes or many pteridophytes such as lycopods and
selaginellas.
The leaves of mosses and liverworts are also often called micro-
phylls but they are not homologous either to the microphylls of
pteridophytes or even to each other. They share the characteristic
of typically arising in three ranks from a tetrahedral apical meris-
Figure 3.26. The origin of
tem cell. The existence of a group of thalloid liverworts (Fossombro-
leaves as flattened lateral branch
systems – megaphylls. niaceae) with the thallus lobed and folded into leaf-like structures
has suggested a mode of origin of liverwort leaves from a thallus or
vice versa. The leaves of liverworts lack the central thickened midrib
(costa) that is observable in many moss leaves, although only in some
does this appear to have a vascular function. The leaf trace arising
from the midrib of the leaf may only just penetrate the cortex of
the stem. Even in Polytrichum, a moss with a relatively well-developed
water conducting system, some of the leaf traces do not connect with
the conducting tissue in the centre of the stem. The leaf trace may act
as a kind of wick or be simply for anchorage and support of the leaf.
The lamina of moss and liverwort leaves is typically very thin, usually
comprising only one cell layer, but several mosses show considerable
complexity in leaf structure.
Figure 3.27. Phyllodes in
‘True’ leaves of higher plants such as angiosperms are thought
Acacia.
to be megaphylls, but, as we saw with the phyllomorphs of the
3.8 CONCEPTUALISING PLANT FORM 127
3.8.4 Phyllotaxis
Phyllotaxis is more useful as a means of describing axial development Figure 3.28. Cladodes of (a)
than as an explanation of organogenesis. There is nothing inherently Ruscus; (b) Phyllonoma.
mystical or mathematical about this process. Phyllotaxis, by the con-
straints of geometry, symmetry and space-filling is by default often
a spiral or helix. This patterning is particularly apparent in plants
with compressed internodes (i.e. high-order phyllotaxis) such as Cras-
sula spp., pineapples, pine cones, etc., and in the arrangement of other
parts of plant such as the tubercles of cacti (Figure 3.30). It is erro-
neous to think of this pattern as the result of an intrinsic genetic or
generative spiralling, although in some plants there is a secondary
twisting of the stem, but these later movements are normal in all
plants.
Phyllotaxis is described by several rather esoteric terms that reflect
the pattern produced by the regular production of leaf primordia at
the shoot apex. The rate of initiation and growth of the leaf primor- Figure 3.29. Arrangement of
dia, and the timing of the plastochrons, determines the phyllotaxis or leaves on a stem: spiral (left)
arrangement of leaves on a stem. The patterns that result often form opposite and decussate (right).
beautiful logarithimic spirals, and are called parastichies. They are, in
reality optical ‘illusions’ produced by the juxtaposition of appendages
produced at regular intervals round the perimeter of the elongating
stem, a direct result of the apical processes.
There are usually two sets of intersecting parastichies. The sec-
ondary connecting parastichies between plastochrons in different
turns of the spiral are usually more obvious than the primary
sequence. Plants produce both right- and left-handed primary paras-
tichies. The angle between primordia in the parastichy tends towards
137.5◦ , the so-called golden section or Fibonacci angle, especially
where the primordia are packed closely together. The golden section
produces the most even and gradual division of the apical dome,
128 ENDLESS FORMS?
is still obvious in the terminal parts of the branch system. The mod-
ular construction is also difficult to observe in some highly modified
forms and in thalloid plants. Nevertheless, the value of describing
plant form and growth in terms of a modular construction is empha-
sised by physiological experiments, which have shown that most of
the energy that goes into producing a reproductive structure comes
from the close vicinity of its own module, rather than translocated
from elsewhere in the plant.
There is a distinction between modules that have terminal repro-
ductive structures (hapaxanthic) or lateral reproductive structures
(pleonanthic). The former have determinate growth. They cease to
grow after a while, often after producing a reproductive structure.
The others have indeterminate growth. The axis is potentially immor-
tal. A whole plant may be determinate or indeterminate or an indeter-
minate plant may have a mixture of determinate and indeterminate
axes.
A difference in branch systems that is often observed is that
between long and short shoots. The short shoots have short internodes
and limited growth, whereas the long shoots have longer internodes.
Some conifers such as Larix and Cedrus have shoots that can switch
between long- or short-shoot growth. Differently shaped leaves may
be produced by each kind of shoot. Short shoots may be produced
as laterals on a long shoot or, in sympodial systems, by the replace-
ment of the forward growth of a shoot by a lateral. The terminal part
of the original shoot then has very short internodes: it is the short
shoot, and the branch system is therefore said to be plagiotropic by
apposition.
Plants are often described, particularly by ecologists, by differ-
Figure 3.31. Larix decidua foliage
showing long shoots and needles ences in the way they are constructed. These differences reflect dif-
clustered on the short shoots. ferences between unitary and modular construction, but in reality
there is every gradation between the two extreme types. In those
that possess unitary construction there is a closed growth because
of a determinate number of parts, the kinds of parts (organs) usu-
ally being numerous and diverse with a marked division of labour
between them. In contrast, in those plants with modular construc-
tion there is open growth because of an indeterminate number of
parts, the kinds of parts are usually few and one part may have a
diversity of functions because of organisational plasticity.
Branching can take different patterns along the plant axis, and
form different patterns of overall form (Figure 3.32). Hallé and Olde-
man, in their studies of plant architecture, have most clearly devel-
oped the idea that plant architecture is under genetic control. Accord-
ing to these authors the architecture of a plant is the momentary
expression of a growth plan, and the architectural model is the result
of the ‘genetic blueprint’ that ultimately determines that growth
plan. They believe that, if the form of a plant is regarded as the
visible expression of its genes, it will surely be most clearly expressed
in a ‘standard’ environment. However, it is difficult to determine just
exactly what a ‘standard’ environment is for a given species. Can it
3.8 CONCEPTUALISING PLANT FORM 131
be exactly defined and is it the same for all members of the same
species?
So far, we have been discussing the architecture of the above-
ground parts of the plant. There are great difficulties in classifying
root systems because of their plastic development. The endogenous
origin of roots allows a very flexible pattern of branching, which is
part of the great plasticity of the root system as a whole. The earliest
plants lacked roots. Early root systems were rather shoot-like, more
tightly constrained, more modular, in their form. The freedom from
constraint of modern root systems, their adaptability, is an aspect of
their specialisation and it defies a simple categorisation.
and organs are usually studied in isolation and organisms have all
but disappeared as fundamental entities in modern biology. While it
cannot be denied that this methodology has been highly successful,
it has limited application when we try to understand the dynamics of
cybernetic living systems such as individual plants, populations and
ecosystems, and it may not be sufficient for a more complete under-
standing of reality. The world in which we find ourselves is not an
inert or mechanical object but a living, open dynamic landscape.
Perhaps the most logical way to conceptualise plants within
their environment is to view them within a holarchy, starting with
ecosystems and descending through a series of further holarchies,
each of which contains a nested reticulum of complexity levels or
holons. At the level of the individual plant (which is not always
recognisable as such) the network embraces, in descending order, the
organs, tissues, cells, organelles, molecules, etc. We stress the integra-
tion of plant parts, such as cells, tissues or organs, rather than treat
them in isolation. Plant morphology therefore cannot be divorced
from plant physiology, but are two dynamic interacting components
of the same living phenomenon. The whole plant, in turn, cannot be
divorced from its ecology. We need to be able to think in four dimen-
sions to understand the multi-layers of complexities within natural
systems, whether it be at the level of the community or at the level
of the cell. The central concept of a holarchic organisation is the set
of relationships that determine or characterise the system. For some
Organisms are better viewed as a botanists, organic form is synonymous with process.
continuous flowing process of The organism has no static qualities or properties. It is a complex
unfolding which encompasses the process of flow, not a thing. A categorisation of processes may be as
entire unbroken movement from important as a categorisation of parts. Continuum or process mor-
fertilisation to death, a movement phology acknowledges gradations between typical structures. Homol-
which initiates similar movements ogy then becomes a matter of degree. By ‘form’ we mean the totality
such as reproduction.
of morphological expression found in plants, not just external appear-
Rolf Sattler
ance but anatomy as well. Such expression surely has greater meaning
within a general theory of biological evolution that embodies change
over time.
Plant morphology can be seen as a discipline that can be carried
in the direction of population biology to the extent to which the
plant can be considered a ‘metapopulation’ of either meristems or
some other developmental or structural unit, and in the direction of
ecology to the extent to which shapes are adaptive. Because process
morphology may be approached at various nested complexity levels
in a continuum, from molecules to ecological levels of the plant com-
munity, it is a more appropriate method for the study of evolution
and phylogeny than typology, but applying it may be more difficult.
Despite the efforts of Hay, Mabberley, Jeune, Sattler and
Rutishauser towards a more dynamic concept of ‘continuum’ or pro-
cess morphology with degrees of homology, much of descriptive plant
morphology is still based on a limited set of empirically based rules.
Although their ideas and efforts are highly imaginative and provide a
better way of seeing plant morphology as a dynamic flowing process,
FURTHER READING FOR CHAPTER 3 133
The trio of sex, multiplication and dispersal are the pillars of the evo-
lution of life on Earth. Multiplication comes through the processes
of sex and dispersal but requires neither. Many organisms reproduce
only, or mainly, asexually and have no special mechanisms for dis-
persal. For organisms living in water, dispersal was never much of
a problem. Water currents dispersed them haphazardly. But disper-
sal on the land is a formidable challenge, a cliff that the first land
colonists had to scale. The landscape was only patchily friendly and
even if a foothold could be established the leap from one damp patch
to another was a huge challenge. The plants that first met this chal-
lenge, and the structures they used to do it, their spores, provide the
first record of complex terrestrial life. In colonising the land, plants
transformed it making it an easier place for other colonists.
Evolution has occurred without sex but sex was the triumph of
eukaryotic organisms, vastly increasing their evolutionary potential.
Sex and dispersal are yin and yang, passive and active, incomplete
136 SEX, MULTIPLICATION AND DISPERSAL
without each other. Each has the potential to multiply the organism.
Sex creates and maintains genetic variability among individuals, but
without dispersal it is pointless as the organisms mate with them-
selves or near relatives limiting the expression of their genetic dif-
ferences. While sex creates different individuals, dispersal tries them
out in different situations where they may be adapted. In this way
the rondo of sex and dispersal has been the engine of evolution, an
engine that has shifted gear with every new specialisation.
Plants have an alternation of generations, a heteromorphic hap-
lodiplobiontic life cycle (see Figure 1.23), where the different phases
of the reproductive cycle are adapted for sex or for dispersal. Different
lineages of plants each have a distinct pattern of reproduction that
represents a particular solution of how to maintain genetic diversity
and how to multiply and establish the plant. Key events have been
the evolution of spores, heterospory, seeds, flowers and fruits. It was
the evolution of flowers, that soft machine for sex and dispersal, that
unleashed a bewildering potential for diversity, a rococo of seemingly
endless forms.
The structures described are clearly fitted for their purpose, adap-
tive, promoting sex, multiplication and dispersal; the physical rules
of nature do sometimes channel adaptation in certain directions. A
good example of this is how spore size can be understood in terms
of Reynold’s Law of buoyancy described below. Plants having a sim-
ilar pollination mechanism may become adapted in a similar way
and evolve convergently, but this does not answer why they share any
one particular form. There are many different ways a flower might
be adapted for pollination by a bee, so why are there particular
norms or archetypes that are repeated again and again in different
lineages?
It is not sensible only to dissect the complex form of plants, to
reduce the integrated form of a plant to a set of unitary adaptations,
as if a living organism was a machine in which each part can be
labelled with a particular function. An equally valid part of the story
of plant reproductive diversity is the limitations of form that devel-
opment imposes, and how, when those boundaries are broken, a new
landscape of form becomes available for evolutionary exploration,
permitting new levels of reproductive complexity and sophistication.
4.2 Sex
layer of cells and multiple eggs are produced by subdivision of the (a)
oogonium. Although normally the oogonium is naked in some algae
they may be produced in cavities in the thallus. In some charophyte
algae a kind of surrounding sterile coat is present, but it is produced
by the growth of surrounding filaments with a different anatomical
origin to the oogonium. This seemingly obscure technical difference (b)
is actually highly significant because it is one of the bits of evidence
that indicates that plants may have had a single common ancestor.
Archegonia are strikingly similar throughout plants. Each is made
up of two parts; the lower chamber, called the venter, and the neck.
Archegonia differ mainly in the number of cells of which they are (c)
composed, the relative size of the neck and venter and in whether (e)
they develop from a superficial or deeper cell. An important stage in
the development of the archegonium is the separation of the wall
from the interior cells, freeing its differentiation. The lowest of the
interior cells becomes the single egg. Above it, there is a ventral canal (d)
cell and several neck canal cells. The canal cells disintegrate at matu-
rity to create the canal via which the sperm enters the archegonium.
Archegonia produce a chemical sperm attractant that in ferns can be
experimentally replaced by malic acid.
In seed plants there is an evolutionary trend in the reduction (f)
of the archegonium. A jacket layer of cells surrounds the central (g)
cells. The number of central cells varies. In Ginkgo a large egg cell,
a ventral canal cell and four neck cells but no neck canal cells are
present. In cycads the pattern is similar but a cell wall is not pro-
duced between the egg nucleus and a ventral canal nucleus that is
Figure 4.1. Archegonia: (a)
short lived. Conifers may follow either pattern but frequently have
liverwort – Pellia; (b) fern –
fewer neck cells than Ginkgo. In contrast, in Ephedra there are 40 or Dryopteris; (c) horsetail –
more neck cells. In Gnetum, Welwitschia and the flowering plants no Equisetum; (d) clubmoss –
readily identifiable archegonia are recognisable but the egg nucleus, Selaginella; (e) Isoetes; (f) Ginko;
or egg, is buried in, and surrounded by, other nuclei or cells that (g) Dioon with detail of neck at
cannot be directly related to archegonial wall cells. mature stage.
The male organ is called an antheridium. It consists of a jacket of
sterile cells surrounding the developing sperm. Rather similar look-
ing multicellular gametangia are produced by the alga Chara. The
antheridium usually consists of a spherical or ovoid sac in which
sporogenous cells give rise to many sperm. Antheridia vary greatly in
size between different groups, and the number of sperm produced
by each antheridium varies from hundreds, even thousands, in some
bryophytes and ferns, to only four in Isoetes. In the seed plants there
is no antheridial sac. The antheridium is reduced to only one or two
cells and only two sperm or sperm nuclei are produced.
Several different kinds of sperm are found in different groups. In
whiskferns, horsetails, Isoetes, ferns, cycads and Ginkgo, a multiflagel-
late sperm is produced with the flagella arranged in a spiral around
the pointed end of the rounded cone-shaped body. In the mosses,
liverworts, hornworts, clubmosses and Selaginella there is a biflagel-
late sperm. The possession of a biflagellate sperm may be a primitive
feature because it is shared with many algae. In the conifers, the
138 SEX, MULTIPLICATION AND DISPERSAL
(a) gnetophytes, and the flowering plants the sperm is non-flagellate but
instead the male cells or nuclei are conveyed towards the egg in a
pollen tube in a process called siphonogamy. A pollen tube is also
produced in cycads and Ginkgo but in these groups it has a haustorial
nutritive function and is not directly involved in fertilisation. Instead
flagellate sperm are produced and released into a chamber above the
archegonium. Flagellate sperm have very limited ability to swim but
they have been observed to be splashed distances up to 60 cm by
(b)
rain.
filamentous protonema soon enters a thalloid phase from which the (a)
mature gametophyte then arises.
The reduction of the juvenile protonemal phase is an evolution-
ary advanced feature in bryophytes. In the moss Dicnemon and the
thalloid liverwort Conocephalum, and some hornworts, development
of the adult gametophyte is direct from the multicellular spore. In
most liverworts there is a juvenile filamentous phase but it consists
of only two or three cells. In thalloid liverworts the apical cell of the
protonema divides to produce a quadrant of cells, giving rise to a
plate of cells in which the apical cell of a growing thallus appears. In
leafy liverworts the protonema produces a clump of cells, sometimes (b)
called the sporeling, from which the mature liverwort arises.
The diverse leafy or thalloid adult gametophytes of bryophytes
are described in Chapter 5. They bear archegonia and antheridia
either separately or together, sometimes with organs such as sterile
hairs called paraphyses or a cup-shaped ring of leaves (perichaetium --
female apex, perigonium -- male apex) that help trap water. Rain drops
splash sperm from one plant to the next. In some complex thalloid
(c)
liverworts sperm transfer is aided because antheridia and archegonia
are raised up on mushroom-like stalks.
Smallness in mosses, liverworts and hornworts is a specialisa-
tion enabling a rapid life cycle to take advantage of transient but
abundant water. Many can then dry out to rehydrate rapidly when
water becomes available again. Many bryophyte habitats have been
created by the evolution of other large plants that have provided Figure 4.3. Reconstructions of
shade or places for the bryophyte to grow as an epiphyte or epiphyll. gametophytes from Devonian
Bryophytes dominate these niches that require smallness. It is intrigu- fossils: (a) Lyonophyton; (b)
ing that evolutionary reduction in the three bryophyte groups, liver- Kidstonophyton; (c) Langiophyton.
worts, hornworts and mosses, which have long separate evolutionary
lineages, has led to evolutionary convergence, so there is a resem-
blance between the leafy gametophytes of mosses and liverworts, and
between the thalli of the hornworts and thalloid liverworts respec-
tively. One subclass of mosses, the Buxbaumiidae, is very interesting
because it shows a great reduction of the gametophyte.
It is this same evolutionary path (where the sporophyte is large
and the gametophyte inconspicuous) that the non-bryophytes have
taken. There are three main growth forms of gametophyte in lycopods,
and in ferns and their allies. The gametophyte may be green and
grow at the soil surface like a very simple thalloid liverwort or horn-
wort; indeed it is often called a prothallus. Most ferns have a gameto-
phyte like this (Figure 4.8). Alternatively, as in many lycopods, the
whiskfern and adder’s-tongue fern, it is a subterranean tuber-like
structure that is usually associated with a fungus (mycotrophic) and
lives saprophytically. The distinction between these two types is not
sharp because small amounts of chlorophyll may be found at the
apex of these mainly saprophytic gametophytes if they are exposed Figure 4.4. Leafy moss
to the light, and green thalloid gametophytes often also have a fun- gametophytes (Polytrichum) with
the sporophyte growing up from
gal symbiont. A third kind, found in all ‘higher’ plants, the gym-
them.
nosperms and flowering plants, is so small that it develops only
140 SEX, MULTIPLICATION AND DISPERSAL
plant spores. Fossils from the Late Silurian and Early Devonian show
a remarkable diversity of sporangia.
(b)
Figure 4.12. Sori showing protective flap called the indusium: (a) section through a
(a) (b) Dryopteris sorus; (b) ‘false indusium’ of Adiantum; (c) Fern leptosporangium in spore
release.
are left as a tattered collar around the base of the seta. In some liv-
erworts like Marchantia the capsules are elevated not just on the seta
but, because the whole sporophyte arises from a stalked platform that
is part of the gametophyte and is called the archegoniophore. In most
liverworts the capsule is spherical or ovoid. The wall of the capsule
may be unistratose, or multistratose. Accompanying the spores in the
liverworts there are sterile cells called elaters that promote dispersal
(see Section 4.5.1).
The capsule splits longitudinally, either regularly or irregularly,
along lines of weakness, into valves, although in some an apical open-
ing is produced. In Asterella a cap called the operculum falls off. In
Cyathodium, tooth-like structures are present around an apical open-
ing. In some liverworts like Monoclea the capsule is elongated and the
capsule splits by a single longitudinal slit. In Riccia there is no seta
and no elaters, and the spores are released by the capsule disintegrat- Figure 4.15. Moss capsule.
ing.
In mosses the seta elongates before the capsule has matured. The
archegonium splits open in such a way that the top part, called
the calyptra, is carried up as a kind of a hat over the apex of the
capsule. Here it continues to influence the development of the cap-
sule until it shrivels and falls off. Moss capsules are complex (Figure
4.4). Often they have a basal sterile photosynthetic region called the
apophysis. Here there are stomata connecting with intercellular air
spaces between the photosynthetic cells. The apophysis can make a
considerable contribution to the energy budget of the sporophyte. The
sporogenous part of the capsule has a central core of non-sporogenous Figure 4.16. Spores with elaters
tissue called the columella, which runs through the centre of the from Equisetum.
spore mass. At the apex of the capsule a ring called the annulus
is present forming an obvious junction with the operculum. Below
the operculum, in the class Bryopsida, there is a simple or complex
peristome. Sphagnum lacks a peristome but has an operculum that is
exploded off to release spores.
(a) (b)
Figure 4.19. Pinus male cones: (a) clusters of male cones (notice arrangement of
needles on short shoots); (b) section showing microsporangia.
Heterothally
The horsetail Equisetum is homosporous but heterothallic, partially
herkogamous and dichogamous. It produces spores of only one size
4.3 DISPERSAL 145
Heterospory
By about in the Middle Devonian, 386 million years ago, plants such
as Chauleria clearly had two sizes of spore produced in different
sporangia: megaspores produced in megasporangia and microspores
in microsporangia. Heterospory evolved several times in distinct lin-
eages in Devonian plants. This can be traced from homosporous
to strongly heterosporous forms in the calamites (fossil relatives of
Equisetum). For example, Calamostachys binneyana is apparently homo-
sporous, although this fossil may be the microsporangiate cone of a
heterosporous species where no megasporangiate cones have yet been
discovered. C. americana is certainly heterosporous with megasporan-
gia containing megaspores three times as large as the microspores
in the microsporangia borne on the same cone. In Calamocarpon the
megaspores are relatively larger again and each megasporangium con-
tains only one spore.
146 SEX, MULTIPLICATION AND DISPERSAL
Endosporic development
Megaspores are produced in smaller numbers than microspores but
their greater size enhances the survivability of the (female) game-
tophyte, maximises the production of eggs and enhances the early
life of the sporophyte after fertilisation. A trend in reduction of the
number of megaspores produced in a sporangium can be observed
in the fossil record. Heterospory in living plants is invariably asso-
ciated with the phenomenon of endospory whereby the micro- and
megagametophytes germinate within the spore and hardly extend
their growth outsde the spore wall. Endosporic gametophytes are
largely non-photosynthetic and depend on a readily available supply
Figure 4.23. Endosporic of nutrients from within the spore itself.
gametophyte (section) in This is the case in Selaginella and Isoetes where the female game-
Selaginella with rhizoids arising tophyte scarcely breaks free of the spore wall, merely sending some
from the surface (cell wall shown rhizoids out to absorb moisture. There is a period at first of free
in black). Three microspores are
nuclear divisions and then apical nuclei become separated from each
shown to the same scale.
other by cell walls. At the tri-radiate apical scar the spore wall splits
4.3 DISPERSAL 147
open and rhizoids grow out. The female gametophyte protrudes from
the megaspore but usually it remains non-photosynthetic, relying on
the nutrient reserves in the undifferentiated mass below. Archego-
nia develop in the surface layer of the exposed region. The male
gametophyte also has greatly reduced requirements. The microspore
is tiny and produces a male gametophyte that consists of only a single
antheridium. When the antheridium is mature it disintegrates and
the spore wall ruptures to release the sperm. One consequence of Figure 4.24. Isoetes after
fertilisation showing the
endospory is an accelerated gametophytic phase, thereby shortening
gametophytic tissue surrounding
the vulnerable sexual phase of the life cycle. the embryo sporophyte. The spore
The nourishment of the female gametophyte may be more pro- wall is still present at the base.
longed if the megaspore is not released and remains within the
megasporangium so it can be fed by the sporophyte.
(a) establishment of the seedling. The simplest pistil types, most like
(b) a folded leaf, become fruits called follicles that split open to
release their seeds. The silique or silicula present in the Brassicaceae
(Figure 4.34) arises from a pistil of two fused carpels.
The rose family Rosaceae exhibits a wide range of fruit types.
The subfamily Spiroideae has one to many dehiscent follicles. Some
(c) (d)
species have winged seeds. The cherries, peaches, almonds and plums
(subfamily Prunoideae) have a single superior carpel with one ovule
producing a fleshy drupe. The inner part of the pericarp is scle-
renchymatous giving the familiar stone of these fruits. The subfam-
ily Rosoideae is very variable. They have single-seeded indehiscent
fruits. In Acaena these are achenes with the calyx modified as long
(e)
hook-tipped spines. In Alchemilla the style is basal. The fruits are often
combined with other fleshy tissue derived in different ways. In the
rose, Rosa, and the strawberry, Fragaria, the fruits are hard achenes,
although in the former they are contained within the fleshy swollen
hypanthium forming the hep, and in the latter the achenes are situ-
Figure 4.35. Some different ated on the exterior of a swollen torus. In Rubus, the blackberry and
ovary and fruit types in the raspberry, the fruits are fleshy themselves, drupelets (little drupes)
Rosaceae: (a) follicles in Filipendula; grouped together on the torus, to give the ‘berry’ (drupecetum). In
(b) perigynous achene in Alchemilla; both Fragaria and Rubus there are a large number of carpels that are
(c) drupecetum in Rubus; (d) berry arranged spirally on the extended torus. In Rosa and Fragaria there is
in Cratageus; (e) drupe in Prunus
one ovule per carpel, in Rubus there are two but only one develops.
cut in half to show hard endocarp.
Subfamily Maloideae has an ovary produced below the petals (inferior)
with 2--5 carpels, producing a fleshy pome. They exhibit a condition
called pseudosyncarpy. The carpels are free on their ventral (inner)
surface but held together by the fleshy fruit tissue.
female and male gametophyte. The other trend is the recruitment (a)
of more and more layers of tissues exterior to the sex cells in the
development. This is exemplified in the evolution of ovuliferous cone
scales and of the carpel. The whole process of sexual reproduction
has been compressed back, so gradually earlier developing vegetative
organs are incorporated and transmogrified into parts of the sexual
apparatus as integuments or the ovary.
In the gymnosperms the megasporangium/nucellus is relatively
well developed with several cell layers (Figure 4.36). Female game- (b)
tophyte development usually begins with a free nuclear phase and
then cell walls are formed. The size and number of nuclei that are
produced varies between groups. In some cycads the ovules are up to
6 cm in length and between 1000 and 3000 nuclei have been counted.
(c)
In Ginkgo there are up to 8000 nuclei, and 2000 in the conifer Pinus.
This free-nuclear phase may last for a considerable time. In Pinus there
is a halt at the end of one season, at the 32 nuclei stage, and nuclear
division resumes in spring. Cell-wall formation begins at the periph-
ery of the coenocytic gametophyte and proceeds centripetally. In the
(d)
cycads and Ginkgo regular hexagonal shaped cells called alveoli are
produced. After cellularisation some of the cells at the micropylar
end become archegonial initials. The number of archegonia produced
varies considerably. Only two are produced in Ginkgo, usually between
2 and 6 in cycads, and sometimes many in conifers.
The flowering plants show several reductions on this pattern.
(e)
Although a similarly multistratose nucellus, is present in many, espe-
cially primitive flowering plants that are termed crassinucellate, more
advanced flowering plants are tenuinucellate and have a nucellus
with a single layer (unistratose). This distinction provides one of the
most important characters in flowering plants separating the two (f)
major eudicot groups, the Asterids (tenuinucellate) from the Rosids
(crassinucellate).
In some ways it is the parallel of the evolution of the distinction
between eusporangia and leptosporangia that separates primitive and
modern ferns. The tenuinucellate condition is very strongly associated (g)
with another kind of reduction because, whereas most crassinucellate
flowering plants have two integuments surrounding the ovule, most
tenuinucellate flowering plants have only one.
As the ovule matures in most flowering plants, the nucellus dis- (h)
integrates, except in a few mainly primitive families like the Piper-
aceae and the more advanced Caryophyllidae where it is retained as
a ‘perisperm’.
→
Figure 4.36. Sexual development of the female tissues of the conifer Pinus is shown in:
(a) young cone with pollen grain inset (not to same scale); (b) section through
megasporophyll; (c) developing female gametophyte at end of meiosis showing linear
tertad of megaspores (detailed); (d) pollination, germinated pollen on nucellus with
pollen tube; (e) linear megaspore tetrad; (f) multicellular female gametophyte before
fertilisation; (g) at fertilisation showing large two large archegonia; (h) female cones in
Pinus aristata.
152 SEX, MULTIPLICATION AND DISPERSAL
4.4.2 Pollination
Figure 4.38. Monosporic (left)
In many gymnosperms, including Pinus, a viscous drop first catches
and tetrasporic (right)
the pollen grains and then, as it is reabsorbed, they are drawn
development of the female
through the micropyle into the pollen chamber above the nucellus. gametophyte (embryosac) in
Only in a very few flowering plants pollen is caught by a liquid trap flowering plants.
although this arises from the stigma. Normally the stigma is dry
although the pollen may be ‘sticky’. In gymnosperms, once the pollen
has been drawn into the pollen chamber, the pollen grain germinates
and a pollen tube is produced, which grows into the nucellus. In
154 SEX, MULTIPLICATION AND DISPERSAL
cycads and Ginkgo the pollen tube is branched and purely haustorial,
providing the male gametophyte with nutrients. In Ginkgo and the
cycads the pollen tube gradually digests the tissue of the nucellus,
finally breaks into the archegonial chamber, a space lying above the
archegonia, and releases the motile sperm (Figure 4.39).
In conifers the pollen tube is initially branched and haustorial
but develops eventually to transfer the sperm nuclei to the archego-
nium. In some species of Pinus there is a period of over a year between
pollination and fertilisation. The development of a pollen tube may
have allowed the nucellus to act as an anti-pathogen screen, recog-
nising the pollen tube with its sperm nuclei and allowing it to grow
but screening out the hyphae of pathogenic fungi. Perhaps it is in
this self-recognition process that sexual-incompatibility between dif-
Figure 4.40. Pollen ferent species and self-incompatibility within a species has its ori-
development (microsporogenesis):
gins. In Pseudotsuga, pollination is dry and the pollen tube conveys
simultaneous on the left,
the male gametes from the integument lobes all the way to the
successive on the right.
archegonium.
Flowering plants are siphonogamous. The pollen grain germinates
Siphonogamous = passage of
directly on the stigma, usually producing only a single pollen tube,
male gametes to the ovule by a
but in most of them the pollen tube is not haustorial; instead, it grows
pollen tube.
down the style. In the angiosperm family Malvaceae both haustorial
and absorptive pollen tubes are produced. Usually only 12--48 h may
elapse between pollination and fertilisation. However, in some trees
such as Quercus and Corylus from seasonal habitats, pollen tube devel-
opment may be arrested for weeks or longer after a period of initial
growth.
Two types of stigma have been described in angiosperms, called
‘wet’ and ‘dry’. A ‘wet’ stigma produces an exudate (cf. pollen drop of
gymnosperms) that helps to attach the pollen grain to the stigma but
seems primarily to hydrate the pollen grain, providing a medium for
pollen tube growth and prevents the stigmatic papillae from drying
out. Pollen tubes penetrate the middle lamellae at the base of the
stigmatic papillae and enter the stylar tissue. Pollen attaches to a ‘dry’
stigma with pollenkitt, a glue-like coating of lipoprotein derived from
the tapetum. ‘Wet’ and ‘dry’ stigmas are associated with gametophytic
and sporophytic self-incompatibility respectively (see below).
4.4 FROM SEX TO ESTABLISHMENT 155
Figure 4.42. Pollination in flowering plants, from the top left clockwise is male
development and anticlockwise is female development.
egg grow up to meet the pollen tube. In conifers, Ephedra, and Gnetum
the pollen tube grows right up to the egg (siphonogamy). In flower-
ing plants the pollen tube enters the embryo sac via one of the cells
beside the egg (a synergid) that has a special receptive filiform appa-
ratus. Then both sperm are released by a pore in the tip of the pollen
tube. They migrate, and fuse, in a double fertilisation, one to the
egg, the other to the polar nuclei, with the formation of a diploid
zygote (sperm nucleus plus egg) and a triploid endosperm nucleus
(male gamete plus two polar nuclei).
Many diverse patterns of embryogenesis have been described. In
Ginkgo and the cycads there is a period of free nuclear division, pro-
ducing up to 256 nuclei, before cell walls are formed to create a
suspensor and proembryo. In the conifers the free nuclear stage only
produces four nuclei before cell walls are produced. Transverse divi-
sion of these first four cells produce two or more layers of cells with
four cells in each layer. These are a proembryo and a suspensor. The
suspensor elongates to push the tiered proembryo into the tissue
Figure 4.44. Embryogenesis in of the female gametophyte, which is then digested by the growing
the cycad Encephalartos, at first embryo. The four suspensor cells, and the embryo cells attached to
coenocytic and then with tiered them, may separate so that several individual embryos may be started
development. (cleavage polyembryony). This is in addition to the potential existence
of several different embryo developments, each the product of the
fertilisation of a different archegonium. However, normally only one
embryo reaches maturity in each seed.
Eventually the embryo differentiates an embryonic root, the radi-
cle, at the suspensor end, and an embryonic shoot at the other end,
called the plumule, which consists of a hypocotyl bearing two to sev-
eral cotyledons. In flowering plants embryogenesis is said to be direct
because there is no free-nuclear phase (Figure 4.43).
This is one of the several characteristics that allow angiosperms
to complete the reproductive phase of their life cycle very rapidly.
Figure 4.45. Embryogenesis in The zygote divides to produce a two celled proembryo. Cell divisions
the conifer Thuja. The long are regular, with cell walls formed at each stage. The terminal cell of
suspensor pushes the embryo into the proembryo divides to form the embryo. The basal cell divides to
the heart of the gametophyte.
produce the suspensor, which connects the embryo to the seed wall.
In some angiosperms the basal cell also contributes to the formation
of the embryo. This happens more often in species that produce large
seeds.
4.4 FROM SEX TO ESTABLISHMENT 157
rate (RGR) and soon catch up in size with bigger seedlings from
larger trees. But, in the smallest gaps where PAR is insufficient these
seedlings remain tiny and are suppressed by competition.
around them and it has been suggested that volatile terpenes are
responsible.
Ferns and horsetails provided the herbaceous vegetation before
the evolution of herbaceous flowering plants. In the Jurassic, in some
habitats Equisetum was dominant. Some horsetails such as E. arvense
are still troublesome weeds. They have deep growing rhizomes that
can grow over a metre below the soil surface and that fragment
easily.
Grasses are now the overall champion as lateral spreaders. They
are highly competitive sward formers. They produce a fibrous shallow
adventitious root system and spread by rhizomes and stolons at the
soil surface or rhizomes in the soil. These readily produce new shoots
called tillers. Different species have different patterns of growth. The
sand couch grass Elymus farctus and the sea lyme grass Leymus are-
narius, which colonise embryonic dunes, have remarkable abilities
(a) to spread laterally but restricted in growing vertically if buried by
sand, unlike the marram grass Ammophila arenaria, which can grow
vertically and horizontally up to 1 m a year in growing dunes. The
deeply buried parts of the plant die. The clover, Trifolium repens, has a
guerilla kind of growth form. It produces stolons which can quickly
(b) ramble through the sward to find openings where it can root, and
most importantly where it can get light. It is commonly overtopped by
grasses.
Specialised vegetative propagation is particularly common in the
bryophytes, many of which reproduce sexually only very occasionally.
Gemmae are the asexual propagules of some liverworts and mosses.
The thalloid liverworts Lunularia and Marchantia have gemma cups in
which small disc-shaped gemmae are produced. Each gemma has a
(c) characteristic notch at the apical meristem. Blasia has a flask-shaped
organ inside which gemmae are budded off. They are extruded from
the flask when mucilage in the flask takes up water. Following release
each gemma produces some rhizoids and grows into a new thal-
lus. Riccardia produces two-celled gemmae within thallus cells. Each
gemma is released when the containing cell wall breaks down. Some
leafy bryophytes also produce gemmae. They arise on their leaves, at
(d) the apex or costa, or on the stems or rhizoids.
The moss Aulocomnium androgynum produces a stalk with a spheri-
cal mass of gemmae at its tip. Some pteridophytes also produce gem-
mae. They arise on the developing prothallus of Psilotum, Tmesipteris
and epiphytic Lycopodium. Many ferns, some club mosses and flower-
ing plants, produce bulbils that may arise in different positions, on
Figure 4.48. Vegetative the margin or lamina of the leaf as in Kalanchoe and many ferns, or on
propagules (gemmae) in the axil of the leaves as in Saxifraga granulata. The bulbils may remain
bryophytes: (a) at the apex of like small tubers or gemmae until after they are shed, or they may
shoots in leafy liverwort develop precociously into tiny plantlets with a swollen base and roots.
Calopogeria; (b) at tips of leaves in In some Allium species bulblets are produced in an umbel on a scape,
moss Ulota; (c) gemma cups in in the same position as florets. They either fall off or remain attached
liverwort Lunularia; and
until the wilting of the frond or stem brings them into contact with
(d) Marchantia.
the soil.
4.5 DISPERSAL MECHANISMS 161
(a)
4.5 Dispersal mechanisms
Bouyancy
The aerial motion of diaspores is related to the Reynolds number (Re) Figure 4.50. Action of Frullania
which is a calculated from the velocity of the object (vp ), the length elaters catapulting spores from the
of the object (l) and the kinematic coefficient of viscosity of the air capsule. The capsule splits open in
lobes; elaters attached to the
(V); Re = (vp l)/V. Pollen, spores and dust seeds are so tiny that they are
capsule wall are stretched and
well within the range in which the viscous forces of air are dominant.
then spring free, so catapulting
They have terminal velocities less than 100 mm/s. There is a change in spores out.
the speed of airflow from zero at the surface of an object to ambient
wind speed at a certain, quite small distance.
The morphology and density of spores and pollen grains may be
affected by the humidity of the air. It seems that many grains become
flattened as they lose water on leaving the sporangium or anther.
Possibly they are adapted to collapse and reinflate on landing as they
rehydrate prior to germination. Large and low-density spores or pollen
grains will be more easily lifted from the sporangium or anther and
will settle or collide more easily with a receptive surface but small,
light spores and pollen grains will travel further before settling. These
requirements are in conflict. These constraints explain the narrow
size range in wind-dispersed spores or pollen grains. Figure 4.51. Action of capsule
Wind-dispersed seeds and fruits are normally much larger than in Sphagnum in spore release. The
spores and pollen except for the dust-like seeds of orchids and par- operculum explodes off, shooting
asitic flowering plants. The tiny seeds of parasitic plants such as out the spores when the capsule
Orobanche, which are produced in huge numbers, 2000 in each capsule, shrinks in maturity.
may be only 200 μm long. They have a testa with ridged reticulations. (a)
Orchid seeds range in weight from 0.3 to 14 μg. They are produced in
huge numbers, up to several million per capsule. (b)
Large wind-dispersed seeds and fruits generally have adaptations
to slow their speed of fall; for example, the parachute-like pappus of
dandelions, Valeriana and Clematis, or the unilateral winged fruits, the
samaras that make the seed or fruit twirl or spin like a helicopter, as (c)
in many species of the families Aceraceae (maple, Acer) and Oleaceae
(ash, Fraxinus). In the lime (Tilia) and hornbeam (Carpinus) there are
bracts connected to the fruit, which act as the rotor. It is the legume
itself and not the seed that is winged in the South American tipu tree
(Tipuana tipu). The Pinaceae (pines, spruces etc.) have winged seeds
with a papery wing derived from part of the ovuliferous cone scale.
Flutterers tend to have a wing that forms a kind of skirt around the
seed or fruit. Most remarkable perhaps are the symmetrical wings Figure 4.52. Autochory,
that allow the seed or fruit to glide like a plane. Alsomitra macrocarpa, explosive release of seeds: (a)
an Asian climber, produces seed in great pendulant gourds. Each seed Impatiens; (b) Viola; (c) explosive
berry of Ecbalium, the squirting
has a wingspan of more than 10 cm and glides through the air when
cucumber.
it is released.
164 SEX, MULTIPLICATION AND DISPERSAL
(h)
(f)
(d)
(b) (j)
(a)
4.5.2 Water dispersal
In several different lineages of plants there has been a return to dis-
persal by water. This form of dispersal was particularly significant
for early heterosporous plants since the large megaspore is most effi-
ciently dispersed by water. Even today heterosporous ferns are mainly
aquatic. Several different kinds of heterosporous plants of the Car-
boniferous coal swamps presumably had water dispersal. Lepidocarpon
is a fossil cone scale that acted first as a wing or parachute and then
(b)
as a float or sail for the megaspore. The descendants of these Car-
boniferous trees, Isoetes, might also use water for dispersal, but the
sporangia are often half buried in mud and it has been proposed
that they may be dispersed by earthworms. There is, however, signif-
icant fragmentation of Isoetes swards by autumn and winter storms,
(c)
so dispersal of megaspores may be effected in this way.
Many aquatic plants reproduce mainly by asexual fragmentation.
When they have been introduced into new areas they have often
spread rapidly asexually. For example a female clone of Elodea canaden-
sis was introduced to the British Isles in 1836 and within a few
decades was choking canals and other waterways. Hydrilla, from the
Old World, introduced to the Americas, and Lagariosiphon, from South
Africa, introduced to New Zealand, have a similar kind of history and
have become nuisance weeds. The water-lilies Nymphaea and Nuphar
have rhizomes with adventitious roots, thus aiding the vegetative
Figure 4.55. Hydrochory,
spread of the plant and providing anchorage. Genera such as Pota-
dispersal of seeds and fruits by
mogeton, Vallisneria and Cryptocoryne propagate by runners, or, in the water: (a) Lodoicea maldavica,
case of Sagittaria, by side shoots. In a few genera such as Aponogeton, double coconut; (b) Cocos nucifera,
adventitious plantlets form on the inflorescence. In temperate regions ordinary coconut, showing inner
most of these aquatics enter a period of dormancy in the winter. Food seed surrounded by fibrous
storage occurs in the rhizomes (Nymphaea), in tubers (Sagittaria and endocarp (left) and section
Aponogeton) or in turions (Hydrocharis, Potamogeton). through fruit (right); (c) Entada
Water dispersal of seeds and fruits is termed hydrochory. Water- gigas, sea-bean fruit and seed.
dispersed fruits and seeds are relatively large or even very large. The
double coconut Lodoicea maldavica weighs up to 90 kg and contains a
two-lobed seed 50 cm long. It floats but is killed by prolonged exposure
to seawater. Coconuts of Cocos nucifera are one-seeded drupes. The fruit
wall, the pericarp, has a skin-like exocarp, a fibrous mesocarp that
provides buoyancy, and a hard endocarp with three pores. The seed
testa, a thin brown layers adheres to the endocarp. The endosperm
is abundant with a white outer zone, the ‘meat’, and a liquid centre,
the coconut juice or ‘milk’. The embryo is at the base. Another case
of gigantism is Entada gigas, a woody climber that produces legumes
12 cm across and more than 1 m long. The fruit breaks into floating
segments, each carrying a buoyant seed 6 cm × 5 cm, which drop
into streams. It was the observation of the seeds on the beaches of
the Azores that is supposed to have prompted Christopher Columbus Figure 4.56. Vivipary in the
to attempt to find their source the other side of the Atlantic. Water- mangrove Rhizophora: the embryo
germinates precociously and the
dispersed seeds and fruits have buoyancy because of the presence of
hypocotyls expand spear-like in
air chambers, either as part of the fruit as in Xanthium, or pseudo- order to plant the seeding.
fruit as in Atriplex, or in the testa as in Menyanthes. The box fruit
166 SEX, MULTIPLICATION AND DISPERSAL
between them. Most have tiny and highly reduced unisexual flowers,
in some cases consisting of a single stamen or pistil. The breakdown of
hermaphroditism is more prevalent among fully submerged aquatics
than in any other group of flowering plants, and intermediate stages
such as monoecy and dioecy (e.g. Vallisneria spp.), are present in many
species. About half are dioecious. The flowers of Ceratophyllum are so
small and reduced that it was once thought to be very primitive.
Most water-pollinated species utilise the water surface for polli-
nation, which has the advantage that, being just two-dimensional, it
enhances the chances of the pollen contacting a stigma. The female
flowers are produced at the surface on long thin stalks which often
reach disproportionate lengths to reach the surface. In Ottelia spp.
these elongated peduncles elevate both hermaphroditic and female Figure 4.58. Inflorescence of
flowers to the surface, which are then pollinated by insects. There- aquatic weed Zannichellia: the male
and female flowers are highly
after, the peduncles spiral and pull the developing fruit under the
reduced.
surface. Vallisneria is dioecious, and, as in Ottelia, the peduncles
may spiral to pull the developing fruit under water. Callitriche (Cal-
litrichaceae) hedges its bets and has underwater surface or aerial
pollination.
Floating male flowers occur in some genera of the frogbit fam-
ily (Hydrocharitaceae). In Lagariosiphon and Vallisneria the erect male
stamens act like miniature sails so that the male flowers are blown
like little sailing ships towards the tethered female flowers. Near the
female flower the suface of the water is depressed by surface tension,
and the male flowers slide down the female, up-ending and deposit-
ing sticky pollen. Enhalus produces similar male ‘boats’ that become
trapped within the perianth of the females as the tide falls. In Hydrilla
the pollen is released explosively into the air to reach the stigmas
of female flowers and is destroyed if it contacts the water. Ruppia
(Ruppiaceae) has bisexual flowers and either underwater or surface Figure 4.59. Inflorescence of
pollination. Ruppia frees air bubbles from its submerged anthers, Zostera: female flowers in detail
showing simple forked stigma.
trapping the pollen on their surfaces. The flowing water waves the
flowers across the stream surface to collect pollen. Anther bubbles
are also released by water-pollinating Potamogeton species. The bizarre
behaviour of the male flowers takes another turn in the hornworts
(Ceratophyllum spp.). Ripe stamens detach themselves from the male
flowers and float to the surface where the pollen is released. Pollen
then slowly sinks to come into contact with the stigmas of female
flowers. Zannichellia pollen also sinks onto the funnel-shaped stigmas
of female flowers in this manner.
Pollen is normally positively buoyant and sometimes hydrophobic.
At the surface pollen grains commonly adhere to each other in rafts.
In three related families Cymodoraceae, Posidoniaceae and Zoster-
aceae pollen grains are elongated like noodles increasing their chance
of catching on the stiff stigmas. As soon as they contact the stigma
they curl around it. In the Hydrocharitaceae and Zannichelliaceae
the pollen is strung together in mucilaginous chains or surrounded
by a flat mucilaginous raft. Thalassia produces mucilagenous strands
of pollen at the surface but these sink in the waves to reach the
submerged stigmas.
168 SEX, MULTIPLICATION AND DISPERSAL
Primary attractants
pollen and spores
Pollen was probably the attractant in early flowers. Insect-dispersed
spores and pollen grains may be sculptured and coated by a sticky
material secreted by the tapetum and called the pollenkitt. Some
species have pollen held together by viscin threads derived from the
Figure 4.60. Multiple stamens anther in various ways. This is sticky and helps it adhere to the bodies
of pollen flowers: (a) connate of insects. Many flowers produce an excess of pollen as a food for the
stamens forming a staminal tube in
pollinator. Pollen is a highly nutritious food and has been found to
Malva (Malvaceae); (b) stamen
have 16%--30% protein, 1%--7% starch, 0%--15% free sugar, 3%--10% fat
bundle in Hypericum (Guttiferae);
(c) branched stamen in Ricinus
plus vitamins. The high nutritional value of the pollen provides the
(Euphorbiceae). energy for pollen to germinate and grow but it is also a rich reward
for effective pollinators.
Vectors attracted by the provision of pollen include hover flies,
bees, beetles and bats and other small mammals. Pollen is the attrac-
tant in many ‘primitive’ magnolioid flowers but it is the only primary
attractant even in some fairly advanced flowers, such as the rose,
tulip and poppy. The pollen grains of pollen flowers are adapted in
various ways. They are coloured by pigments called carotenoids and
flavonoids that give the mainly yellow colour. The yellow colour is
seen most effectively when it contrasts with a differently coloured
Figure 4.61. Poricidal horned corolla. The pollen of some species is deep red, purple or even blue.
stamens of Vaccinium (Ericaceae). Several different kinds of pollen flowers can be distinguished.
Pollen flowers have many stamens and powdery pollen may be shed
onto the perianth or collected directly out of the anthers as in Arge-
mone and Paeonia. Some, such as Magnolia have numerous stamens
and shed sticky pollen onto the perianth where it is eaten by bee-
tles, whereas others have relatively few but showy stamens. Buzz-
pollinated flowers in some species of Solanaceae, Ericaceae and Melas-
tomataceae have anthers opening by terminal pores. Vibrations and
rhythmic squeezing forces the pollen out. Pollen flowers often mag-
nify the attraction of their stamens by producing accessory organs
4.5 DISPERSAL MECHANISMS 169
that mimic the stamens. Sterile stamens (staminodes) are quite com- (a)
mon. The Melastomataceae have dimorphic stamens, the outer showy
staminodes and the inner ones fertile. Some Lecythidaceae such as
Couroupita have sterile stamens fused into a ligule arching over the
pistil. Another feature often observed is a textured or bearded region
of the corolla coloured like the stamens and advertising the availabil-
ity of pollen.
(b)
ovules or seeds
Another kind of primary attraction is the provision of ovules or seeds.
This is very common where the visitor is being attracted to disperse
the seed. Seeds are produced in much larger quantities than required
and many are sacrificed to an animal visitor so that a few can be
dispersed. It is a kind of tax on reproduction to ensure dispersal.
Only a few plants provide ovules as the primary attractant at the (c)
stage of pollination. These plants are said to have brood-place blos-
soms. In these species there is a rather constant relationship between
pollinator and flower. The yucca has large flowers in which the sta-
mens are kept well clear of the stigma. The female yucca moth Tegetic-
ula yuccasella lands on a flower and hooks itself onto a stamen. It col-
lects pollen with two prickly mouthparts and then flies to another
flower. First, it establishes whether it has been pollinated, and if not,
pushes some pollen into a tube formed by the three elongated stig-
mas. Then it lays an egg in one of the ovary locules. It repeats this
process a few more times and then flies off to another flower. The Figure 4.62. Pollen flowers: (a)
moth larva develops within the ovary, eating some seeds, but a pro- Hypericum (Guttiferae), (b)
portion of the seeds survive. Eventually the moth escapes by chewing Argemone (Papaveraceae) (c)
a hole in the ovary wall. Couroupita (Lecythidaceae) with
The figs, Ficus (Moraceae), may represent the most extraordinary showy staminodes.
reversion to insect pollination in the angiosperms. Some primitive
species in the family are wind pollinated. They have small flowers
aggregated into a head. In the 500 or more species of fig, the head
has invaginated to form a bottle-shaped syconium with the florets on
the inside. Some specialised florets provide brood places for species-
specific gall wasp larvae. Inside the syconium, there are male, female
and sterile flowers. The sterile flowers have short styles enabling the
female wasp to reach the ovary to lay its egg with its ovipositor. These
flowers are on a longer peduncle so that to the gall wasp all stigmas
appear to be at the same level. The wasp larvae develop to maturity
inside the fig. They give rise to wingless males and winged females.
The males never leave the fig but fertilise the females before they
depart. On leaving the fig the female gall wasps collect pollen from
the male flowers. They find another fig at the right stage and pollinate
all the female flowers inside, before laying eggs in the short-styled
ones.
Animal dispersal of seed and fruits is called zoochory. Zoochory is Figure 4.63. The Yucca flower
very common and predominates in some habitats such as moist and (Agavaceae) provides ovules/seeds
to attract pollinators; it has a
wet tropical forests, heathlands and grasslands. The evolution of the
glandular stamen and grooved
fruits of flowering plants may have provided an important new kind
pistil.
of high-energy food especially for small mammals and birds.
170 SEX, MULTIPLICATION AND DISPERSAL
nectar
Many species pay an indirect tax on reproduction by providing nectar
as an alternative food to pollen. In the early stages of the evolution of
Figure 4.67. Nectaries have
flowering plants the stigmatic exudate may have provided the attrac-
different forms, from breaks in the
tant but in most nectariferous living flowers nectar is produced by
epidermis to modified stomata.
specialised nectaries. At its simplest nectar is exuded onto the surface
of the disk or petal but it may also be stored in various pouches or
spurs. Nectar can be exuded from the epidermis through the cuticle,
through thin cell walls and in places where the epidermal cell wall
(a) (b)
and cuticle is incomplete, or through special pores that are often
situated at the end of the phloem strands.
Petal and tepal nectaries are commonly associated with a corolla
spur or a pouch that may not be nectariferous itself but collect nectar
produced by the disk or stamen. There is large variation in the length
of any spur. Some orchids have extraordinary long spurs. Perhaps the
longest are those of Angraecum sesquipedale from Madagascar which
has spurs more than 40 cm long. It is visited by a hawkmoth with
an extraordinary long proboscis. Stamen nectaries are provided as
staminodes or as modified filament bases. The tubular honey leaves
of Helleborus in the the buttercup family are fundamentally modi-
fied staminoids. In buttercup itself (Ranunculus) the staminoidal petals
retain a cup-like nectary at the base. Nectariferous appendages of the
stamens reach into the spur in Viola. Disk nectaries are very common Figure 4.68. Flowers with spurs
in which the receptacle has a conspicuous ring between the stamens or honey leaves: (a) Angraecum
and the pistil that glistens with nectar. Septal nectaries are present sesquipedale with a spur up to 40
in five different super-orders of monocots including the amaryllids, cm long; (b) Helleborus honey
bromeliads and gingers. The nectariferous region is found in a groove leaves are modified staminodes.
or pocket between the septa of the locules of the ovary. The nectary
connects to the outside by a slit or pore at the base of the style.
They are absent from most lilies and orchids, which have a nectarif-
erous perianth. Nectar may be exuded by specialised hairs (trichomes),
which are often found in tufts. This type of nectary is relatively rare
and is confined to a few families.
Nectaries outside the flower are commonly associated with main-
taining a population of ants that protect the plant but in some spe-
cialised inflorescences like the cyathium of the spurges Euphorbia, the
extra-floral nectaries do attract pollinators.
Sugar concentration varies between about a quarter and three-
quarters by weight. There are three main types of menu on offer. Some
plants like Berberis and Helleborus produce a nectar that has mainly
sucrose. Others produced a balanced menu with sucrose, fructose and
glucose in roughly equal proportion. Abutilon is like this. Some large
and relatively advanced families like the cabbage, carrot and daisy
families (Brassicaceae, Apiaceae and Asteraceae) produce nectar that Figure 4.69. Septal nectaries in
Asparagales, seen in transverse and
has low sucrose but high fructose and glucose composition. Different
longitudinal sections of the pistil.
species of rhododendrons produce each kind of menu.
172 SEX, MULTIPLICATION AND DISPERSAL
fruits
Another kind of secondary attractant is the fleshy tissue present in
fruits. Fleshy fruits of several different sorts have been categorised on
the basis of the anatomy of the pericarp. Three anatomical regions are
present in the pericarp: an outer exocarp, an inner endocarp and the
mesocarp between. There are also specialised multiple pseudofruits in
the flowering plants in which the fleshy tissue is at least in part com-
Figure 4.72. Resin-producing
posed of the receptacle, stem and/or bracts. Two contrasting examples
flower of Clusia.
are the pineapple and the fig.
There are 250 000 species of flowering plants. To a very large extent
the diversity of flowers is expressed in the way they advertise them-
selves to animal pollinators. Vectors are initially attracted to flowers,
and guided within them, by various kinds of advertising and sign
posting. We can thank the secondary attractants of scent, colour, and
shape for their wonderful beauty and diversity.
mimic the smell, colouration and texture of rotting meat. The world’s
largest flower Rafflesia arnoldii, which is up to a metre across, is polli-
nated by flies attracted by the smell of carrion and its blotchy appear-
ance. The flies make their way to the underside of the disk where
polysporangiate anthers smear a pollen mush on their backs.
Many aroids or arums produce scents of carrion, dung or urine,
to attract the pollinators, which are mostly flies. The spadix has cells
which are packed with mitochondria. Respiration can significantly
raise the temperature, up to 16 ◦ C above ambient in Arum. The raised Figure 4.74. The orchid
temperature mimics that of the rotting animal products and also Pleurothallis raymondii with paired
drives off the scents effectively. orbicular osmophores (scent
Insects may be attracted by the warmth of a flower. In arctic and wands).
alpine regions flowers are heliophyllous so that the flower follows the
sun, focusing its rays within the corolla. Mosquitoes bask at the focal
point of the flower. Patterns of heat distribution within the flower
may help direct the pollinator towards its centre after arrival at the
flower.
Scent and heat production are often closely associated. The water-
lily Nuphar raises the temperature of its flowers to 32 ◦ C over a four-day
period. Flies and beetles are attracted by an evaporating scent and
then trapped in a kind of chamber roofed by the enclosing tepals.
The insects are highly active on the warm dance-floor provided, and
by accident first pollinate and then get covered by pollen before they
are released. The flowers of species of Annona, the soursop and custard
apple are also strongly warmth producing. Again, beetles congregate Figure 4.75. Carrion flower of
in the warm flowers at night-time to mate. Male flowers cease to be Stapelia. This flower produces a
foetid smell of rotten carrion that
warm first, so that beetles move on to the female flowers to keep
is attractive to flies.
warm and thereby carry out pollination.
Figure 4.77. Anthocyanidin the presence of flavone or flavonol co-pigments, a chelating metal,
pigments are widespread in plants. carotenoids, an aromatic acyl or sugar substitution, or a methylation.
Differences in flower pigments exist at various levels in the taxonomic
hierarchy. A well-known example is the presence of a unique set of
pigments, the betalains, in 10 families of the Caryophyllales (Cen-
trospermae), a characteristic that, among others, links such diverse
families as the Cactaceae, Aizoaceae, Chenopodiaceae and Amaran-
thaceae.
Colour patterning helps direct pollinators to the centre of the
flower; many are not visible to our eyes but show up in the UV spec-
trum. There are stripes that lead to the centre, like the lights leading
to an airport runway. These ‘honey guides’ are particularly prominent
in bee flowers. Alternatively, the centre of the flower where the nectar
is provided may be marked out like a bull’s-eye. Dark stamens may be
Figure 4.78. Visible spectrum of silhouetted against a lighter-coloured corolla.
bees (A), birds (B) and humans Petals have textural patterning, mattness or shininess or even
(C). Both birds and bees are directional brightness. A common pattern is the possession of conical-
sensitive to the ultra-violet, but
papillate epidermal cells, like blunt projecting cones which maximise
birds are more sensitive at longer
the reception of low-angle light and evenly spread light reflected back
wavelengths.
from the mesophyll. Surface microsculpturing adds guide lines.
In some flowers other visual cues on the plant signal the status
of the flower, for example in epiphytic Columnea florida (Gesneriaceae)
the flowers are inconspicuous but just before flowering two translu-
cent red spots or ‘windows’ appear on the leaves, and are conspicuous
to hummingbirds approaching from below. In the West Indian Mar-
cgravia sintenisii (Marcgraviaceae), which is visited by hummingbirds,
honeycreepers (Coerebidae) and todies (Todidae), the nectaries are at
first yellow but turn bright red when the flower opens.
Both insect and vertebrate eyes are attuned to detecting move-
Figure 4.79. A betanidin ment. One interesting kind of patterning is the chequer-board pattern
pigment: betaxanthin. Betanidins
seen in many fly-pollinated flowers such as Fritillaria and Oncidium. It
are found in only a small group of
is thought that this pattern creates an optical illusion of movement
Caryophyllid families.
because of the insect’s compound eye. Possibly the arrangement of
4.6 THE DIVERSITY OF FLOWERS 177
florets. In this region there are female florets that are receptive to
the pollen the flies have carried from other plants. Later, the midges
are allowed further up into a region where there are male florets.
Here they are covered with pollen before the outer curtain of sterile
florets withers to allow their escape. Alocasia and Colocasia, taro and
cocoyam respectively, attract beetles and flies into the chamber and
trap them there overnight when the neck constricts. Amorphophallus
titanum, over 2 m tall, which is pollinated by large beetles, prevents
their escape from the region of the spadix by an overlapping ledge
around the rim of the spadix and by the smooth walls of the spathe.
They only escape when the spathe disintegrates. The effectiveness of
pit traps is often magnified by scented and optical trickery.
Optical traps have evolved in several different families often com-
Figure 4.89. Pit trap in Arum
bined with rings of hairs that temporarily prevent exit from a pol-
maculatum. A curtain of sterile
linating chamber. They have a dark chamber whose entry is visible
flowers in the throat of the spathe
prevents the escape of pollinators from the outside but is hidden in darkness from the inside. Instead,
until the female flowers have been the pollinators are confused by translucent windows in the wall of the
pollinated and the male flowers chamber. There has been remarkable convergence between Aristolochia
have shed their pollen. (Aristolochiaceae) and Ceropegia (Asclepiadaceae) in this respect. In
Dutchman’s pipe, Aristolochia, the curved perianth tube attracts polli-
nators in but confuses them so that they fly or climb up towards the
anthers and stigma. In Ceropegia the lantern-like upper part of the
flower allows the pollinator in, and downward pointing hairs and
a translucent lower chamber encourage it down to the anthers and
stigmas.
Lobster-pot traps like that in Calcyanthus have many tightly over-
lapping tepals which form a cone like a lobster-pot trap. Tiny beetles
are attracted in between the tepals by scent to eat the food bodies
produced on the tips of the tepals and then find they cannot get
out because of stiff downward pointing bristles. They are forced fur-
ther and further in towards the receptive stigmas; 2--3 days later the
Figure 4.90. Ceropegia staminodes bend to cover the stigmas, while the stamens release their
encourages pollinators to enter its pollen onto the beetles. Then the tepals then bend back to release the
chamber by patterns of light and
beetles.
shade, and discourages their
A liquid trap is produced by the water-lily Nymphaea. The cup-
escape with downward-painting
hairs.
shaped stigma exudes a pool of sugary liquid to form a liquid trap.
Insects carrying pollen land on the upright immature stamens and
slide off into the pool where some of them drown. The pool evaporates
or is reabsorbed so that the bodies of the insects float down with their
pollen onto the stigma. Later the stamens fold over the stigma and
release their pollen.
Booby-trap flowers in the broom and gorse, Cytisus and Ulex, have
a staminal tube and style forming a stiff spring depressed by the keel;
the insect landing on the keel causes it to split, releasing the style and
stamens explosively (Figure 4.92). One of the most bizarre pollination
Figure 4.91. Lobster-pot trap; mechanisms is utilised by the tropical mistletoes (Loranthaceae). The
Calycanthus. The tightly overlapping petal lobes of the tubular corolla are joined at the tip. They become
tepals allow only entry into the
increasingly turgid as the flower matures until, at the slightest touch
flower until they reflex to open.
by a visiting bird (usually a flowerpecker: Dicaeidae), it bursts open
4.6 THE DIVERSITY OF FLOWERS 181
violently, and the stamens, which are adnate to the corolla, inflex or
recurve sharply, showering the bird’s head with pollen. At the same
time the style snaps to one side to prevent self-pollination.
Tender traps lure their victim with the rich scents of sex or food.
Some species of orchid have encouraged faithful pollination by mim-
icking the female of their male pollinator so that the bee attempts to
copulate with the flower. Drakea, the dragon orchid, is an Australian
orchid that has a labellum mimicking a female wasp. As the male
wasp lands on it the labellum swings forward banging the wasps head
against the anther or stigma. Pseudo-copulation is a common polli-
nation mechanism, well known in the European flora because of the
different species of Ophrys (bee-orchid), each resembling a different
pollinator. There is no food reward for the provision of nectar would
encourage the bee to visit every flower in an inflorescence leading to Figure 4.93. Trip flower; Drakea
self-pollination. A scent or wax is provided, which may act like an mimics a female wasp and flips the
insect pheromone. Euglossine bees collect droplets of perfume from male against the anther and
the surface of the flower and store it in their hollow hind legs. stigma.
Tender traps have the advantage that male bees searching for a
female to copulate with are likely to range widely and are more dis-
cerning of shape and scent than they would be if looking for food,
so that cross-pollination is encouraged. A different example of ten-
der trap appeals not to the sexual appetite of the pollinator but to
its hunger; for example in Arisarum proboscideum the spadix is spongy
and white like the underside of a fungus, and gnats are attracted and
congregate inside the spathe.
flies attempt to lay their eggs on the flower surface. Syrphids (hover
flies) have a long proboscis and mimic bees and wasps. They can gain
nectar from tubular flowers and can also eat pollen when it is mixed
with saliva. They are common visitors to the yellowish, whitish and
pinkish umbels of ivy (Hedera), Cornus, Viburnum, and elder (Sambucus),
and species of the Apiaceae (Umbelliferae). Bee flies mimic bumble
bees and are common visitors to inflorescences with many tiny flow-
ers like willow and thyme.
A range of other insects are pollinators. Heather (Calluna vulgaris) is
visited by a wide range of large pollinators and is an important source
of nectar for honey production but is also pollinated by a species of
thrip, 1 mm long, which is so tiny it lives most of its life within the
flower. Several can be found in a single flower. The females fly between
flowers to mate effecting cross-pollination. They lay their eggs at the
Figure 4.100. Fly-pollinated
base of the corolla and the larvae mature there over winter but leave
flowers of Deherainia smargdina
(Theophrastaceae) have a fetid
to pupate in the soil. Calluna can also be pollinated by wind.
smell and are green. The flowers Wasps will visit a wide range of relatively open flowers. A few
are protandrous; the stamens lie (Polistes) have specialised mouthparts. Species which are wasp polli-
close to the stigma at first but nated are often ‘brown’ and have a fruity scent. Gall wasps are impor-
spring back before the stigma tant for fig pollination and some are fooled by Ophrys species.
becomes receptive. Cantharophily or beetle pollination is relatively unspecialised.
The beetles scramble around relatively large bowl-shaped flowers or
inflorescences of small closely aggregated flowers and are as likely to
eat and destroy floral parts as eat nectar or pollen. They are attracted
by sweet scents. Flowers are pale or dull and floral adaptations include
having many relatively broad stamens. Weevil-pollinated flowers are
more specialised. They have a narrow entrance to a chamber within
which the weevils may live. The flowers of Victoria amazonica behave
in a fascinating, if bizarre, way. During the first night, at sunset, the
flowers open. At this stage, the petals are shining white and attract
Figure 4.101. Viburnum has an scarab beetles which are trapped at around midnight when the petals
umbel in which showy sterile close. One to two hours later, the flower begins to change colour to
flowers surround the fertile a delicate pink. By sunrise the following morning, it is closed com-
flowers. pletely. The colour gradually deepens to a rich purple and, by mid
afternoon, the flower re-opens, although the staminode chamber con-
taining the beetles remains closed. At sunset, on the second night,
the flower reopens, the beetles fly off to repeat their nocturnal feast-
ing and, in so doing, pollinate a fresh flower. During their exit they
pick up pollen on their bodies now sticky from a night of gorging
on the sugary exudates of the flower’s carpels. Thereafter, the flowers
submerge and the seeds ripen under water.
Bird pollination or ornithophily is especially important in the
tropics. Hummingbirds, honeyeaters, sunbirds, lorikeets and others
are all important pollinators. Flowers are often bright red or yellow
but lack scent (Figure 4.103). Bird-flowers have a tremendous diversity
Figure 4.102. Thrip-pollinated of form, pattern and colour but, for descriptive purposes, they are
Calluna. It is also pollinated by bees often classified into five basic types: gullet, tubular, brush, capitate
(producing a honey that flavours
and spurred (Figure 4.103). Flowers are commonly simply tubular and
the liqueur ‘Drambuie’) and is also
more or less polysymmetric but some like Erythrina have a large flag.
pollinated by wind.
Nectar guides are not usually present but the perianth may have
4.6 THE DIVERSITY OF FLOWERS 185
flowers in the dry season. Several aquatic plants are regularly cleis-
togamous but at least one of these, Subularia, has been observed to
produce open flowers on a dried up lake margin. In addition to vege-
tative propagation, Lobelia dortmanna is able to adopt several sexually
reproductive strategies. Normal out-crossing aerial flowers are visited
by numerous small insects. However, the inflorescences of those indi-
viduals that grow in deep water cannot break the surface, and there-
fore they develop cleistogamous flowers. In 1847, Sir Joseph Dalton
Hooker reported on the strange mode of pollination found in the
mudwort (Limosella aquatica) on Kerguelen Island. In winter, in two
feet of water, beneath the ice, it was found to have fully formed flow- Figure 4.110. Andromonoecy
ers in which pollination had occurred. An air bubble was generated in Aesculus: hermaphrodite and
male flowers are produced on the
in the space between the over-arching petals, and, within this air
same tree.
pocket, the pollen was transferred to the stigma.
Reproduction in flowering plants is a two-stage process, pollina-
tion followed by fertilisation, while mechanisms to ensure cross-
fertilisation are of two sorts: those that promote cross-pollination,
usually by the physical or temporal separation of male and female
parts of the flower, and those that prevent self-fertilisation by a
chemical/physiological self-recognition after self-pollination called
self-incompatibility.
Only about 4% of flowering plants are dioecious, with separate
male and female individuals. There are also monoecious species, with
separate male and female regions (diclinous). Interesting interme-
diate conditions like andromonoecy, male and bisexual regions on
the same plant (as in Aesculus hippocastanum, horse chestnut) or gyn-
(a) (b)
odioecy, separate female and bisexual plants (as in some species of
Ficus) are also found. Gynomonoecy is associated with the speciali-
sation of different flowers within the capitulum in the daisy fam-
ily, the Asteraceae: outer petalloid flowers are female (or sterile) and
inner flowers are bisexual. There are regional and ecological dif-
ferences in the rate of dioecy: only 2% of the British flora is dioe-
cious and 12% of the New Zealand flora. In temperate regions wind-
pollinated flowering plants tend to be dioecious or monoecious and
diclinous.
Where dicliny is associated with insect pollination nectar is usu-
ally the attractant but Decaspermium parviflorum is a dioecious Indone-
sian species that provides sterile pollen in the female. It is impor- Figure 4.111. Dioecy in Silene
tant that the male and female flowers look identical to the insect dioica. The drawings show the
so that it does not discriminate between them. Sterile stamens are female flower (a) and male
flower (b).
found in female Silene dioica, which also compensates for its lack of
pollen by the production of more nectar. In the Cucurbitaceae, in
which there are closely related monoecious and dioecious species,
the stigma is lobed and somewhat reminiscent of the three stamens
of the male flower. Dioecious species in the tropics are more often
insect pollinated than those in temperate regions. They tend to have
large animal-dispersed seeds and it is possible that dioecy in them is
the result of competition between the sexes within plants. In dioe-
cious species male plants sometimes produce more flowers and grow
188 SEX, MULTIPLICATION AND DISPERSAL
the vast diversity of flower shapes, colours and scents that encourages
effective cross-pollination. An important factor in their speciation
has been pollination with pollinia. This very effectively multiplies
and stabilises new variants. Orchid pollination biology, with its abil-
ity to seemingly make endless forms, mirrors one of the most effec-
tive methods of old-fashioned plant breeding to create new cultivars;
crossing two genetically different variants and then creating a diverse
range of distinct cultivars by selection and inbreeding. The evolution-
ary dance is made manifest and in this family there do seem to be
endless forms of flowers!
arrow on the paths; some are two-way, but many are mainly or only
one-way. Some paths are busy avenues of evolution that have been
explored time and again. Other streets are quieter and have been
explored much more rarely.
But the metaphor of a city plan of plant form is too static. E. J. H.
Corner in The Life of Plants writes about charting the lost channels
of the delta of biology. Borrowing that image, we can visualise plant
form as channelled between the twin banks of development and adap-
tation. The channels converge and diverge. There are eddies and back
currents. The flow is slow in some channels, in others fast. Different
lineages end up travelling down the same channel. There are two
great rivers of vegetative form, either towards greater woodiness and
growing as a tree, or towards being a herb. There are many tribu-
taries towards specialisations such as being an aquatic, a climber or
a succulent. These channels and tributaries have been explored again
and again in different orders, families, and even genera of plants. It
is this pattern of exploration that represents the archetypes of plant
evolution, not any particular ideal form.
Occasionally the phylogenetic flow breaks through the twin banks
of adaptation and development and floods the plain. When this hap-
pens there is, for a while, no limit on where the flow can go until
new channels emerge or the flood retreats to particular isolated pools.
What we shall see is that some lineages are circumscribed, confined
to particular pools of adaptation and development, but others have
a history of breaking their banks, and exhibit a great diversity of
form. The challenge is to understand the historical reasons for this
difference and to characterise the developmental and adaptive con-
straints on change, but the first step is to delineate the lineages
themselves.
Notice how the names of groups Table 5.1 The hierarchy of taxonomic ranks for plants with the example of
above species each have their a species of wheat and maize showing to which group (taxon) each belongs
own particular ending so that the at different ranks
taxonomic rank can be
recognised. Note too how Kingdom Viridiplantae
superior ranks have the stem Subkingdom Plantae (or Embryobionta)
name of one of the taxa they Division (Phylum) Tracheophyta
include at a lower rank. However,
Subdivision Spermatophytina
this is not compulsory and can
Class Magnoliopsida (or Angiospermopsida)
lead to confusion because
different authors may name the
Subclass Monocotyledonidae (or Liliidae)
same group at different ranks. Order Poales
Alternative names tend to be Family Poaceae
used at higher ranks, but this too Subfamily Pooideae Panicoideae
can get confusing as different Tribe Triticeae Andropogoneae
names are used for exactly the Subtribe Triticinae Tripsacinae
same group. In the text below Genus Triticum Zea
some of the most commonly used Subgenus T. subgenus
alternatives are listed. Above all, Triticum
we should avoid mistaking the
Section T. section Zea section
menu for the meal. Classification
Triticum mays
has its limitations and pitfalls.
Species T. aestivum Z. mays
Subspecies T. aestivum Z. mays
subsp. aestivum subsp. mays
Variety T. aestivum
var. aestivum
deep in the tree were near the surface and visible. This difficulty is
being overcome utilising DNA sequence data variation and computer
based methods of analysis, but it has led to differences of opinion and
different classifications, among taxonomists. The tree represented in
Figure 5.1 is only one version of what is currently thought to be
the arrangement of the major phylogenetic branches of plants. It is
possible, indeed likely, that some of the branches will move position
as more plants are sampled.
The second point is that it is impossible to give a name to every
branch of the evolutionary tree. There simply are not enough tax-
onomic ranks in the taxonomic hierarchy. So taxonomists have to
decide relatively subjectively which branches to honour with a name
and at what taxonomic rank. This is the source of many differences
in the classifications you will observe in different books.
With these points in mind you are now ready to embark on a
journey. It is actually a journey that we should start in the present
day on the smallest twigs, all 350 000 of them, one for each liv-
ing species, and like an army of ants, travel down into the evo-
lutionary tree back in time, but for simplicity let us imagine it
the other way starting on the trunk and climbing in turn up each
branch.
5.1 THE PHYLOGENY OF PLANTS 195
(a)
(a) (f)
(a)
(e)
(c)
(b) (g)
(b)
folding of leaves (Fissidens), and the overlapping of leaves and leaf (a) (b)
bases. Various structures act as wicks, including hairs, divided leaves
(paraphyllia), tufts of rhizoids and tufts of branches. In Aulocomnium
there is a dense felt coating the stem surface. Many ectohydric mosses
have conical leaf cells, which project from the lamina increasing the
surface for wetting. Tortula has papillae that are cutinised and which
shed water into the spaces between them where the water is absorbed. (c)
Many ectohydric mosses are amazingly tolerant of desiccation.
Tortula muralis can survive for 10 months without water and then
revive within a few hours. Tolerance of desiccation is helped if dry-
ing is slow; growing in tight clumps and cushions helps slow dry-
ing. The presence of long, hyaline leaf tip hairs (aristae), as in Rha- (d)
comitrium, also helps. The aristae form points on which dew can form,
and, when dry, they spread out and reflect the sun. Hyaline cells are
prevalent especially in Leucobryum, which has the photosynthetic cells
surrounded by hyaline cells in an analogous way to Sphagnum.
Lycophytina Euphyllophytina
G-type tracheids with a thick decay-resistant inner P-type tracheids with bordered pits and strands of
layer. secondary wall crossing the pores and surrounding the
pits. The secondary wall is laid down discontinuously
separated by areas of primary wall.
Dichotomously branched. Monopodial or pseudomonopodial, with helically arranged
branches.
Kidney-shaped (reniform) and flattened sporangia, Sporangia in pairs in terminal bunches dehiscing through
singly on short stalks in the axils of leaves, with a single slit on one side.
cellular thickening along the line of dehiscence.
204 ORDERING THE PATHS OF DIVERSITY
the stem, with many rhizoids on the lower surface. These early rooting
structures are different from true roots because they lack root hairs
and a root cap. In rhizomorphic lycopods the first branching of the
embryonic shoot produces one upright branch and one positively
geotropic branch called the rhizomorph bearing modified leaves as
‘rootlets’.
Alternative names: Lycopodiaceae Rhyniophytes have a number of features that distinguish them
∼400 species. from the eutracheophytes: a kind of adventitious branching in which
Distinguishing features: small the vascular strand of the branch is not connected to the main strand;
spore-producing plants with an abscission layer at the base of the sporangium; S-type tracheids
sporophyte dominant; with a thin, inner, decay-resistant layer in the cell wall; and a spongy
homosporous; gametophyte small outer layer.
mycotrophic and tuberous.
Life-form/ecology: clubmosses are 5.2.5 Subdivision Lycophytina
widespread from the tropics to There are three main groups: various genera of clubmosses (Lycop-
the arctic. They grow terrestrially sida), Selaginella (Sellaginellopsida) and Isoetes (Isoetopsida). The latter
in wet ground, grassland and as two groups are sometimes placed together in a group called the Ligu-
hanging tropical epiphytes latae because they have a peg-like extension of their leaves called a
(Phlegmarius). ligule that is absent from the clubmosses. They are also heterosporous
Sister groups: Selaginellopsida and and have similar endosporic gametophytes.
Isoetopsida.
Fossil record: the clubmosses are Class Lycopsida -- clubmosses
in some respects our most In all clubmosses the gametophyte is small and relatively insignif-
primitive living plants. Different icant. In some it is lobed and green, in others it is subterranean,
forms look very similar to fossils tuberous or carrot-shaped and mycotrophic (= living in a close asso-
from the Devonian. The simplest ciation with fungi). They have tracheids concentrated usually in a cen-
living kinds are species of tral column of xylem surrounded by phloem (protostele) which may
Huperzia, like the extinct
sometimes be lobed (actinostele) or pleated (plectostele). The sporo-
Asteroxylon from the Devonian
phyte plant bears multiple sporangia on a dichotomously branched
They have fertile leaves,
sporophylls, that are identical to leafy axis. In Palhinhaea it looks like a small branched tree. The stems
vegetative leaves but have are either held vertically upright or hanging, or there is a horizontal
sporangia in their axils. stem at the soil surface (stolon) or in the soil (rhizome) from which
vertical stems arise. Dichotomously branching roots arise at the stele
and, in forms with upright stems, travel through the stem cortex
before emerging some distance from where they originated.
Figure 5.21. Phylloglossum. Figure 5.20. Lycopods: (a) Huperzia; (b) Phlegmaria; (c) Lycopodium.
5.2 THE NON-FLOWERING PLANTS 205
(a) (b)
5.2.6 Euphyllophytes
The earliest known euphyllophyte is the fossil Psilophyton, a small
plant about 50 cm tall, that had profusely branching side branches.
Pertica was similar but taller and more regularly branched.
There are three main subdivisions of living euphyllophytes: the
whiskferns and adder’s-tongue ferns (Psilotophytina), the ferns and
horsetails (Polypodiophytina) and the seed plants (Spermatophytina).
The first two have been placed in a group called the Moniliformopses
because they have a vascular tissue that develops like a necklace, with
the earliest xylem (protoxylem) confined to lobes of the necklace. The
Moniliformopses include extinct early fern-like plants, the Cladoxyli-
dae, Stauropteridae and Zygoteridae. Recently a new arrangement of
living Moniliformopses has been suggested by molecular data, sep- Figure 5.25. Archaeopteris with
arating off the Adder’s-tongue ferns from other ferns but includ- detail of foliage.
ing the horsetails as sister to the remaining ferns. The Spermato-
phytina are placed in a group, the Radiatopses, so-named because
the vascular tissue develops in a radiating pattern outwards from the
centre.
An important group of Radiatopses were the progymnosperms, so
called because they share several features with, and seem to prefig-
ure, the earliest seed plants. For example, Archaeopteris had webbed
side-branches forming leaves or pinnae, the ability to undergo thick-
ening growth, enabling it to grow as a tree, and heterospory. However,
unlike the tree lycophytes, they have a vascular cambium that pro-
duces new tissues on both sides (bifacial).
Distinguishing features: they are
extraordinary rootless plants
bearing rhizoids only on rhizomes.
Branching is by equal forking of
5.2.7 Subdivision Psilotophytina the stems and rhizomes. Psilotum
Class Psilotopsida -- whiskferns has scale-like leaves. In Tmesipteris
There are about 3--8 species of whiskferns. the leaves are broad and flat and
attached to the stems in a peculiar
sideways manner giving the whole
plant a frond-like appearance. The
(a) (b) (c) sporangia are fused together
(synangia) and produced on short
lateral branches. They are homo-
sporous and produce a tuberous
gametophyte not unlike a portion
of the sporophyte’s rhizome
Life-form/ecology: they grow as
epiphytes or on rocks in the
humid tropics and subtropics.
Tmesipteris clothes the trunks of
Nothofagus and tree ferns in New
Zealand and in similar habitats
Figure 5.26. Psilotopsida: (a) Psilotum; (b) synangia (groups of sporangia in the axils of including cycads in temperate
microphylls); (c) Tmesipteris. Australia.
208 ORDERING THE PATHS OF DIVERSITY
(c)
(d)
(a)
Maratiopsda
Figure 5.31. The modern ferns (Polypodiopsida) and their relationship with primitive
ferns (Marattiopsida).
(a) (b)
(a) (b)
(a) (b)
(b)
(a)
or lake margins and produce a creeping rhizome that bears the fronds
and roots at nodes. Marsilea has a four-lobed pinnule and resembles a
four-leaf clover, while in Regnellidium the frond is two-lobed. Pilularia
lacks a lamina to its frond and has a narrow cylindrical leaf. The
Marsileales have bean-shaped sporocarps that are homologous to a
reduced frond. When moistened the sporocarp produces a branched
gelatinous structure bearing sori. The two genera of Salvineales are
Azolla and Salvinea. Azolla has leaves tightly overlapping and fitting
into each other so that they trap a buoyant film of air. Salvinea has
leaves in threes on a branched rhizome: one is finely dissected, look-
ing like a branched root, and acts as a stabiliser. The remaining
two have an upper surface covered with water repellant hairs. They
produce modified sori (sporocarps), producing either microspores or
megaspores that float because of the presence of a frothy massula.
Azolla harbours the blue-green nitrogen-fixing alga Anabaena in a sym-
biotic relationship, and thus has been economically important, espe-
cially to rice production.
Figure 5.44. Ginkgo: (a) tree showing characteristic form; (b) foliage showing long and
short shoots; (c) male catkins; (d) foliage of extinct Ginkgoidae.
Figure 5.45. Cycads with cones: (a) Encephalartos; (b) Stangeria; with megasporophylls
(c) Cycas.
(a) (b)
220 ORDERING THE PATHS OF DIVERSITY
(c) (d)
podocarpales (podocarps)
The podocarps are a sister lineage to the Araucariales and together
with them constitute the majority of the conifers of the Southern
Hemisphere. The female cones generally bear only one or two ovules
surrounded by bracts. The name Podocarpus (‘foot-fruit’) comes from
the fleshy stalk bearing the ovule that becomes fleshy (arillate) in seed.
The male cones are like catkins. Characteristically, podocarps have a
very simple and primitive pattern of branching but this does not pre-
vent them growing as very tall trees emerging above the canopy of
Nothofagus forest in New Zealand, for example. Today they are not nor-
mally dominants but on the rolling fertile lowlands podocarps such as
rimu and totara once formed extensive forests in New Zealand before
they were cleared by the Maori and European colonists. Podocarps
are also an important component of the shrubby vegetation found
at higher altitudes and in areas of disturbance. The related Phyllo-
cladus, with flattened frond like branches, is normally placed in its
own family the Phyllocladaceae.
5.2 THE NON-FLOWERING PLANTS 221
Cupressaceae Taxodiaceae
(a)
5.3 Class Magnoliopsida – flowering plants
There are more than 250 000 species of flowering plant. Alternative
names for them include the angiosperms, Angiospermopsida.
Not all of these features are found in all flowering plants and some
are found in a few other plant groups. Figure 5.53. Floral diversity:
(a) Houttuynia; (b) Aristolochia;
(c) Allium.
5.3.2 Fossil record and origin
The origin of flowering plants, Darwin’s ‘Abominable Mystery’, is con-
jectural. There is scarcely any hard evidence of their origin before
the Cretaceous (135 million years ago) but molecular data indicate a
much more ancient origin for the lineage that eventually gave rise
to flowering plants. There are intriguing fossils of flower-like struc-
tures like those of Archaefructus, an aquatic plant of 124 million years
ago, but the first undoubted flowering-plant fossils are pollen from
equatorial latitudes of the Late Early Cretaceous, 125 million years
224 ORDERING THE PATHS OF DIVERSITY
amborellales
DNA sequence data places a plant called Amborella trichopoda from
(a)
New Caledonia in a basal position as a sister to all other flowering
plants. This is not to say that it is the ancestor of all other flowering
plants. Rather that it is the closest living relative of the ancestor and
like all other living flowering plants it exhibits a mixture of primi-
tive and derived features. It is a shrubby evergreen plant with simple
leaves that may be lobed. It has tracheids but no vessel elements. It is
dioecious with flowers grouped in axillary cymose inflorescences. It
has a perianth consisting of five to eight undifferentiated segments
that are weakly joined at the base and are arranged in a spiral. The
male flower has numerous (10--25) laminar stamens, the outer fused (c) (b)
to the base of the perianth segments. Pollen is aperturate to non-
aperturate and sulcate with a granulate outer wall and is possibly
not tectate, a feature of possibly great significance. The female flower
has five to six free carpels in a whorl. Carpels are open at the tip
Figure 5.57. Amborella: (a) plant;
and have one ovule. Seeds are endospermic and the embryo has two
(b) male flower; (c) female flower.
cotyledons.
228 ORDERING THE PATHS OF DIVERSITY
eumagnoliids
The eumagnoliids include several dicot orders as well as the monocots
(see below). They include many species that exhibit some primitive
features they share with basal monocotyledons: whorls of floral parts
in threes (trimerous), monosulcate/uniaperturate pollen, apocarpous
flowers.
Like the ANITA grade of flowering plants many of these eumagno-
liids are aromatic and include, for example, Lindera -- allspice, Piper
-- pepper, Cinnamomum -- cinnamon, Aniba -- bois-de-rose oil, and Sas-
safras with its scented insecticidal oil. Another useful plant in this
group is Persea, the avocado. Figure 5.60. Chloranthus.
chloranthales
The Chloranthaceae (Figure 5.60) is the only family. It has about 75
species, most in the genus Hedyosmum. They are shrubs, lacking vessel
elements. Their wood is soft and their swollen internodes sometimes
collapse on drying. Flowers are very small and unisexual, with a single
stamen or carpel and with or without a single whorl of three perianth
segments.
laurales (laurels)
There are seven families, most of which are trees, shrubs or lianes
but Cassytha, in the Lauraceae, is a genus of twining, almost leafless
plant parasites like the dodders (Cuscuta). They have flowers that vary
from small to large (Figure 5.61).
magnoliales (magnolias)
Generally small trees or shrubs and lianes, most having relatively
large showy flowers (Figure 5.62). The large flowers have a poorly
Figure 5.62. Magnolia.
differentiated perianth and quite often a variable number of seg-
ments. In addition some have partially sealed carpels and diverse but
commonly broad stamens with a weakly distinguished filament and
valvate anthers.
canellales
There are only two families of evergreen shrubs and trees, the Canel-
laceae and Winteraceae, in the order. Drimys, in the Winteraceae, has
a peppery taste. The flower has variable numbers of perianth seg-
ments, flat stamens with a poorly differentiated filament and only
weakly sealed carpels. The Canellaceae have the stamens fused in a Figure 5.63. Drimys.
ring.
230 ORDERING THE PATHS OF DIVERSITY
5.3.6 Monocots
The monocots represent by far the most evolutionarily successful
lineage of the eumagnoliids and represent about 25% of all flower-
ing plants, about 50 000 species. They are very diverse ranging from
tall palm trees to tiny aquatic plants like Lemna (duckweed). Numer-
ically they might be considered less important than the eudicots,
but they include the grasses that provide the great majority of food
for humans, either directly (wheat, rice, millet, etc.) or by feeding
domestic grazing animals. They are clearly a monophyletic group and
most have:
r single cotyledon
r sympodial growth (the palms Arecales are monopodial)
r linear, parallel-veined leaves in which the leaf base surrounds the
Figure 5.64. Acorus.
stem
r primary root soon aborts and a wholly adventitious root system
develops
r closed vascular bundles and lack of interfascicular cambium
r flower parts in threes
r pollen development (microsporogenesis) successive
r monosulcate pollen
liliales (lilies)
In contrast to the superficially similar Asparagales, the Liliales tend
to have nectaries at the base of the floral parts, spots on the petals
and stamens with anthers opening to the outside (Figure 5.68). Other
features like the cellular structure of the seed coat also link them.
Like the amaryllids they include many geophytes, producing bulbs
(Liliaceae, Melanthiaceae) or corms or rhizomes (Colchicaceae). Some
are shrubby or vines (Philesiaceae, Smilacaceae). They also include
chlorophyll-lacking mycotrophs in the Corsiaceae. There are four
main lineages: (1) Smilacaceae with Liliaceae; (2) Alstroemeriaceae
with Luzuriagaceae and Colchicaceae; (3) Campynemataceae; and
(4) Melanthiaceae.
Figure 5.70. (a) Watsonia, (b) Tulipa, (c) Xanthorhoea, (d) Moraea.
5.3 CLASS MAGNOLIOPSIDA – FLOWERING PLANTS 233
The orchids are the largest family of the order and comprise the
most diverse and remarkable of all flowering plant families with
between 800 and 1000 genera and up to 20 000 species, rivalled in
numbers only by the Asteraceae. Orchid flowers have a complex archi-
tecture and are exceedingly diverse in the structure and arrangement
of the various parts of the column, rostellum and pollinaria and in
the shape, colour, and scent of the perianth. Figure 5.71. Floral diagrams of
the three main patterns of orchid
architecture. The Apostasioideae
are a small SE Asian subfamily with
three stamens. The
Cyprepediodeae are the slipper
orchids. The monandroid orchids
are by far the most numerous and
include several families of both
terrestrial orchids (mainly
Orchidoideae and Spiranthoideae),
and epiphytic orchids (mainly
Epidendroideae) and even lianes
(Vanilloideae).
Commelinids
arecales (palms)
The Arecaceae palms are the most important group of monocot trees
but, like other monocot trees, they are unbranched or only weakly
branched and lack a vascular cambium (Figure 5.30). Rather, sec-
ondary growth occurs by the expansion, and occasional dichotomous
splitting, of a large apical meristem. The leaves of palms are large and
complex, often palmate or pinnately lobed, and highly folded. Their
flowers are relatively simple, following a standard monocot pattern
with parts in threes, but often they are grouped together in massive,
profusely branched inflorescences. About six subfamilies have been
distinguished based on the form of the leaf (fan or feather) and its
folding (rib down -- induplicate, or rib up -- reduplicate).
Most other families in the order have reduced and relatively incon-
spicuous, often unisexual, flowers adapted for wind pollination by
having an inflorescence held on a long leafless scape above the leafy
rosettes. This trend has occurred in several of the constituent lin-
eages. For example, sister to the Xyridaceae, are the mostly wind
pollinated Eriocaulaceae, with similar dense heads of flowers. A few
species in the Eriocaulaceae are insect pollinated with nectariferous
petals. Some species are monoecious with female only marginal flow-
ers in the head and central ones male. Other species are dioecious. In
the Typhaceae the male part of the spadix is above the female. The
Juncaceae have a typical monocot perfect flower, but it has a green
or brown and papery perianth. They are wind pollinated, and a few
Figure 5.76. Xyridaceae.
are dioecious, but some have become secondarily insect-pollinated
although they lack nectaries. In their sister family the sedges, Cyper-
aceae, the perianth is reduced to scales or bristles or is absent. Some
genera, such as Scirpus, have hermaphrodite flowers. Others, includ-
(a) (b)
ing the largest genus Carex, have unisexual flowers with male and
female flowers in different parts of the inflorescence. The male flow-
ers consist only of three stamens with a bract called the glume on the
abaxial side. A glume is also present in the female flower. In addition,
two inner glumes have become fused to form a bottle-shaped perigy-
nium or utricle surrounding the pistil. The style protrudes through
the opening in the utricle.
In the Poaceae, the grasses, the flowers are similarly reduced Figure 5.77. Cyperaceae
and adapted for wind pollination (Figure 5.78). They are grouped florets: (a) female; (b) male.
alternately side-by-side in spikelets. The primitive floral condition
for grasses is retained by the bamboos (Bambusoideae). They have
(b)
simple, often trimerous spikelets and they may have three lodicules
and three stigmas. Progressive reduction has given rise to the stan- (c)
dard grass floret pattern. Ampelodesmus, a primitive member of the
advanced subfamily Pooidae also has three lodicules. At the base of
the spikelet are two glumes that protect the spikelet in development.
Each floret in the spikelet is enclosed by two other bracts; the lower
is the lemma and the upper is the palea. Within the floret there
are usually three stamens and a pistil with two feathery stigmas. At
the base of the pistil there are two tiny lodicules, remnants of the
perianth, which swell to push open the floret or shrink to allow it (d)
to shut. Cross-pollination is ensured not by separation of the sexes
(a)
but by the different time of pollen release and stigma receptivity
and, most importantly, by a unique form of self-incompatibility. The
Figure 5.78. Poaceae: grass
fruit is an achene with the seed fused to the fruit wall (a caryop-
inflorescence: (a) plant with
sis). It is usually shed enclosed within the lemma and palea, which
paniculate inflorescence,
may be modified to aid dispersal. Threshing releases the grain from (b) spikelet, (c) distichous
this chaff. The Poaceae is one of the most successful of all flowering arrangement of florets in spikelet,
plant families because of its ability to spread laterally by rhizomes (d) single floret with three dangling
and stolons or the production of herbivory, drought- and fire-resistant stamens and two feathery stigmas.
tussocks.
236 ORDERING THE PATHS OF DIVERSITY
commelinales (spiderworts)
The Commelinales are mainly herbs like the Haemodoraceae and
Commelinaceae (Figure 5.79) but include the aquatic Pontederiaceae.
Frequently the flowers are zygomorphic (monosymmetric). Hetero-
morphic flowers are found in the Commelinaceae (enantiostyly) and
Pontederiaceae (heterostyly).
zingiberales (gingers)
The Zingiberales may be regarded as plants that do not produce an
aerial stem except when flowering (Figure 5.80). They have showy,
often strongly zygomorphic flowers especially adapted to bird polli-
nation. The form of the flower with a large lip (labellum) is only
exceeded in complexity in the monocots by the orchids. Sepals
and petals are fused (connate) and sterile stamens (staminodes) are
petaloid. The different families illustrate a great variety of special-
isations for pollination in the tropics. The bananas, Musaceae, are
Figure 5.79. Commelinaceae: the largest of all herbs, though they look like trees. The gingers,
Tradescantia gigantia, an upright Zingiberaceae, include more than a thousand species of tropical
form (Enchanted Rock, Texas).
herbs. In some ways the flower is analogous to that of the orchids
with its pronounced zygomorphy and adnation of a single stamen to
the perianth with other stamens converted into tepals and the anther
supporting a slender style. However, the filaments and style are long
and the anthers and stigma are exposed so that the pollinator is not
as effectively ‘controlled’ as in the orchids. The Costaceae have five
staminoids connate as a labellum and the stamen is broadly petaloid.
Pollinators include hummingbirds and large bees. As in the gingers,
the anther supports the slender style. The arrowroots (Marantaceae)
have an asymmetrical flower with a single median stamen, which is
half petaloid and all others are staminoidal and petaloid. The style is
under tension and triggered to scoop pollen from the bee pollinator.
Canna (Cannaceae), or Indian shot, has two whorls of three tepals, and
up to five petaloid staminoids, which are showier than the perianth.
In addition the fertile stamen and style are petaloid.
Basal Eudicots
Basal eudicots such as the Proteales and Ranunculales have a pattern
of leaf venation in which the lateral veins terminate at the margin in
a small tooth (craspedodromus). They have a well-developed perianth
but this is poorly differentiated into a calyx and corolla, and has a
variable number of tepals spirally arranged or in whorls of three. Sta-
mens and carpels are numerous and varying in number. The carpels
are free to connate and have a sessile stigma.
trochodendrales
This order has only two species of evergreen trees from east and South
East Asia each in its own family, Tetracentron sinense and Trochodendron
aralioides (Figure 5.83).
gunnerales
There are only two genera in the order. Gunnera has the familiar, mas-
sive, palmate and deeply ribbed leaves. Usually grown beside water it
is also a colonist of land-slips. One advantage it has is the fixed nitro-
gen it gets from the symbiotic blue-green bacteria (Nostoc) that live
in its exposed roots and rhizomes. It produces large strobiloid inflo-
rescences of tiny flowers, either bisexual or unisexual. Myrothamnus,
from tropical Africa and Madagscar, is a resurrection plant, appear-
ing to dry out but able to revive and start growing again when water
Figure 5.83. Trochodendron.
becomes available.
Core Eudicots
Core eudicots have predominantly flowers with parts in fives (pen-
tamerous) with a clear distinction between calyx and corolla. There
are two main lineages, the Rosids and Asterids, three large basal lin-
eages, the Caryophyllales, the Santalales and the Saxifragales, and a
number of others of uncertain relationship like the Berberidopsidales
and Vitales. These basal orders are crassinucellate (see below).
santalales (sandlewoods)
All five families of the Santalales (Santalaceae ∼500 species, Olacaceae
∼200 species, Opiliaceae 28 species, Misodendraceae 8 species, and
the Loranthaceae ∼940 species) include tropical parasitic species. The
Loranthaceae are the most specialised parasites. The shrubby, liane
or twining habit is common throughout the order. Figure 5.88. Grossulariaceea:
Ribes.
vitales (vines)
This order is of supreme importance to us as the source of wine from
the grape vine Vitis. Many other genera are twining vines with or
without tendrils (Rhoiocissus, Cissus). Cyphostemma is a caudiciform and
Leea a shrub and small tree.
berberidopsidales
This tiny order of two families, one with only one species Aextoxi-
Figure 5.90. Berberidopsidales:
con from Chile and the other with only two genera Berberidopsis and
Berberidopsis.
Streptothamnus from Chile and eastern Australia.
240 ORDERING THE PATHS OF DIVERSITY
5.3.7 Rosids
Rosid orders or even families are very diverse in their floral struc-
ture. Most of the ecologically (and economically) important trees from
forests and savannas around the world are Rosids. They include the
tallest flowering plants such as the eucalypts, the mahoganies in the
tropics, the savanna acacias, and oaks, maples and beech from tem-
perate forests.
Basal Rosids
geraniales (geraniums)
The Geraniales include one large family, the Geraniaceae, and sev-
eral very small ones. One interesting feature they share is the pres-
ence of glands on the margin of the leaf. They have pentamerous
obdiplostemonous flowers with a persistent calyx. The two largest
genera Pelargonium and Geranium produce similar beaked fruits but
differ in the former having monosymmetric flowers and a nectarifer-
ous pedicel (Figure 5.91). The Geraniaceae are commonly herbs with
Figure 5.91. Geraniales:
jointed stems but the other families in the order include shrubs and
Geranium.
trees.
5.3 CLASS MAGNOLIOPSIDA – FLOWERING PLANTS 241
crossosomatales
These are a small order of shrubs and small trees adapted to dry
habitats.
(a)
(a) by scales and have a minute perianth. The strange she-oak (Casuarina)
of South-East Asia and Australia was once considered to be very prim-
itive because of its very simple inflorescence. The flower consists only
of a bract with two scale-like bracteoles with, in the male, a single
stamen and, in the female, a single pistil. Male flowers are aggregated
into catkins and the hard bracteoles of the female flowers form part
of a woody ‘cone’.
(b)
Eurosid II
The Eurosid II clade includes these important orders: Brassicales,
Malvales, and Sapindales.
brassicales (crucifers)
The Brassicales include sister lineages so distinct and without inter-
mediates that one wouldn’t guess their close relationship. The fami-
lies Brassicaceae (crucifers), Resedaceae (mignonette), Limnanthaceae
Figure 5.101. Brassicaceae: (poached-egg flower), Batidaceae (saltwort), Koeberliniaceae (allthorn),
(a) half flower; (b) floral diagram. Setchellanthaceae, Moringaceae (Bennut), Caricaceae (papaya) and
Tropaeolaceae (nasturtium) are very distinct in their floral morphol-
ogy. For example, the Brassicaceae is also called the Cruciferae because
of its cross-shaped flowers of four petals and usually six stamens. In
contrast the Resedaceae usually has six fringed petals and the Tropae-
olaceae has five and also has a long hairy claw. One floral feature that
is present in several families of the order is a nectariferous portion
of the axis below the stamens (androgynophore) or pistil (gynophore).
One of the most significant features these families share is the posses-
sion of mustard oils (glucosinolates). This seemingly obscure chemi-
cal character provides protection against herbivory and fungal attack.
Another interesting feature is the usual lack of mycorrhizae in the
Brassicaceae, perhaps because they tend to occupy relatively nutrient
rich early successional situations.
sapindales (mahoganies)
The Sapindales also include several very important tropical and sub-
tropical families of trees and shrubs such as the Meliaceae (∼575
Figure 5.103. Anarcardiaceae:
species), Sapindaceae (∼1350 species), Anacardiaceae (∼850 species)
Pistacia.
and Burseraceae (∼540 species). They frequently have pinnate or
5.3 CLASS MAGNOLIOPSIDA – FLOWERING PLANTS 245
5.3.8 Asterids
The Asterids are tenuinucellate. Most also have a pentamerous sym-
petalous corolla, and most have an equal number of epipetalous sta-
mens, alternating with the five corolla lobes. This set of attributes
has long been recognized as those of a group called ‘Sympetalae’
(for a tubular corolla of connate (fused) petals). The Asterids con- Figure 5.104. Cornaceae:
tain the most advanced members of the Eudicots, and the most Cornus.
recently evolved. They have diversified especially in having specialised
pollination mechanisms. Floral architecture and behaviour show
many individual adaptations to particular kinds of pollinator.
Basal Asterids
cornales (dogwoods)
The Cornales exhibit a tendency, seen more fully developed elsewhere
in the euasterids, towards the possession of a pseudanthium, a com-
pound inflorescence of small flowers grouped together in a flat head
and made showy in different ways. In Hydrangea, for example, flowers
are in a cymose inflorescence with marginal ones sterile and showy,
and fertile central ones. An alternative pattern is seen in Cornus (Cor-
naceae), which has large, showy, outer bracts like petals around the Figure 5.105. Theaceae:
inflorescence. Although some Cornales have a synsepalous calyx most Camellia.
have free petals. There are three large families in the order, the Cor-
naceae, Hydrangeaceae and Loasaceae, ranging from trees and shrubs
to robust herbs. The Loasaceae have barbed stinging hairs.
ericales (heathers)
The Ericales are a diverse order and include, as well as the heathers
(Ericaceae), other very distinct families such as the balsams (Balsam-
inaceae -- fleshy herbs), the Marcgraviaceae (lianes), the Polemoni-
aceae (mainly herbs, especially of arid areas, but some shrubs and
lianes), the camellias (Theaceae -- shrubs and trees with thick leaves),
and primulas (Primulaceae -- herbs). The brazil-nut family Lecythi-
daceae, and the Sapotaceae, another important tropical family, are
sister families in the order. The latter produces latex and gums, and
includes species such as the chewing-gum plant Manilkara and gutta-
percha plant Palaquium. One lineage of Ericales includes the insec-
tivorous pitcher-plant family Sarraceniaceae (Sarracenia, Darlingtonia,
Heliamphora) and Roridula with sticky resin secreting hairs (but not
Figure 5.106. Primulaceae:
insectivorous) and sensitive stamens, as well as the Actinidiaceae (the
Dodecatheon.
kiwi-fruit or Chinese gooseberry).
246 ORDERING THE PATHS OF DIVERSITY
garryales (silk-tassel)
Aucuba is the commonly grown yellow spotted evergreen ‘laurel’.
Garrya (Silk-tassel Bush) is another commonly cultivated shrub with
showy catkins. It produces highly toxic alkaloids. One rather peculiar
feature of this order is the presence of petroselenic acid as a major
fatty acid in seeds.
have flowers that are usually very strongly zygomorphic and have
either four or two (Salvia) stamens. The four-loculate ovary is divided
into four segments from the top. The style reaches down to the base
of each locule (gynobasic). Each segment is dispersed as a separate
nutlet when the seed is mature. In the Lamiaceae the inflorescence
is a verticillaster with cymose verticals on a main raceme.
The Orobanchaceae, contains most of the parasitic, while the Len-
tibulariaceae and Byblidaceae are insectivorous and have sticky and
digestive glands.
boraginales (borages)
Parallel evolutionary trends can be seen in the related family, the
Boraginaceae. Some borages have an entire ovary like the Verbenaceae
whereas others are like the Lamiaceae with a gynobasic style and four
nutlets. Most have polysymmetric flowers arranged in cymes. Echium
is exceptional with its zygomorphic flower.
Euasterid II
The Euasterid II lineage shows varying degrees of aggregation of flow-
ers into a head in which different flowers may become specialised for
Figure 5.114. Scrophulariaceae: showiness (pseudanthium). They tend to have small epigynous flowers
(a) Digitalis; (b) floral diagram. grouped together in a flat head, exemplified by the umbel of the Api-
ales (umbellifers) and the capitulum of the Asterales (daisies). Some
are woody shrubs or climbers but the majority are herbs.
They have a remarkable chemical diversity especially in com-
pounds that act as herbivore deterrants.
aquifoliales (hollies)
The Aquifoliaceae is by far the biggest family in the Aquifoliales
because of the genus llex (holly) with 400 species of small evergreen
trees or shrubs. Flowers are normally small and unisexual. Most
species are dioecious. Helwingia (three species) and Phyllonoma (four
species) have epiphyllous inflorescences.
the pollen onto the surface of the capitulum. Later the stigmatic lobes
open. The fruit of the Asteraceae is usually crowned by a pappus
derived from the calyx. The pappus in Asteraceae is very variable,
either absent or cup-like, or with scales, bristles, simple or feathery
hairs, which are barbed, or glandular. The fruit, called a cypsela, is a
kind of achene of an inferior ovary. The dispersal adaptations of the
Figure 5.119. Tubular central fruit contribute to the success of many species as weeds.
floret showing inferior ovary and The features described above have evolved in many groups outside
the calyx converted into a bristly the Asteraceae. Many of the structures of a capitulate infloresecence
pappus. found in the Asteraceae are paralleled in other families in the Aster-
ales such as the Goodeniaceae (∼300 species), which has an indu-
sium, the Calyceraceae (∼55 species), Lobeliaceae (∼1200 species) and
Campanulaceae (∼600 species). Phyteuma and Jasione, in the Campanu-
laceae, both have capitulate inflorescences surrounded by an involu-
cre of bracts. Jasione has a kind of primitive ‘pseudo-indusium’ formed
by swollen stigmatic lobes. The one species of the monotypic Brunon-
iaceae, which is remarkably similar in appearance to Jasione and is
sometimes put in the Goodeniaceae, shows a further parallel in hav-
ing an involucrate head, though the head is cymose and the florets
are hypogynous. The piston-like mode of pollen presentation in the
Figure 5.120. Pollen
Asteraceae also has parallels with that in the Campanulaceae (Physo-
presentation mechanism. Florets
plexis) and Lobeliaceae.
are protandrous and the piston
like style pushes pollen on to the The repeated evolution of these features argues strongly that
surface before the stigma lobes they are adaptive. One advantage of having a capitulum, for exam-
open to become receptive. ple, is the protection given to the ovule and seed. Functionally it
provides a large showy target for pollinators and yet each ovule is
packaged separately, as a defence against predators and for disper-
sal. There is a lot of diversity in the size and number of florets that
capitula contain. There are the familiar huge capitula of the sunflow-
ers, which have been selected by plant breeders. At the other end of
the spectrum many species have capitula containing very few florets.
Table 6.1 The life-forms of plants based on Raunkiaer’s system Classification of woodiness
1. Holoxylales
Phanerophytes (trees and shrubs >25 cm tall)
– the whole plant is lignified
Evergreen trees without a bud covering 2. Semixylales
Evergreen trees with a bud covering – plants with the lower
Deciduous trees with a bud covering branches lignified and the
Shrubs 25 cm–2 m tall upper herbaceous
Chamaephytes (woody or semi-woody perennials, with resting buds 3. Axylales
< 25cm above ground) – herbaceous plants
Shrubs or semi-shrubs, which die back to the resting buds Leaf size
Passively decumbent shrubs subleptophyll <0.1 cm2
Actively creeping or stoloniferous (procumbent) shrubs leptophyll 0.1–0.25 cm2
Cushion plants nanophyll 0.25–2 cm2
Hemicryptophytes (die back in harsh season, with resting buds at the nano-microphyll 2–12 cm2
soil surface) microphyll 12–20 cm2
Protohemicryptophyte micro-mesophyll 20–56 cm2
Partial rosette plant mesophyll 56–180 cm2
Rosette plant macrophyll 180–1640 cm2
megaphyll >1640 cm2
Cryptophytes (with buds below ground or in water)
Geophytes Leaf consistency
Rhizome geophyte Malacophyll (soft)
Bulb geophyte Sclerophyll (hard)
Resinous/succulent
Stem tuber geophyte
Water/succulent
Root tuber geophyte
Helophyte (marsh plants with resting buds in water saturated soil)
Hydrophyte (buds in water)
Therophytes (annuals, which survive as seed)
Classification of plants based (plants adapted to dry habitats), halophytes (plants adapted to
on the nature of the shed salty conditions) and epiphytes (plants adapted to grow on other
organ(s) plants). These categories are not exclusive: sea-grasses are hydrophytes
and halophytes, while epiphytes may be xerophytes too. The
Whole plant shedders which
survive as seeds (annuals). Podostemaceae, a peculiar family of aquatics, are more easily char-
Shoot shedders, seasonally acterised by a system designed for the bryophytes.
renewing the whole shoot. Different plant groups with different evolutionary histories have
Branch shedders, seasonally tackled the problems of surviving in diverse ways but these ways are
shedding the upper parts of not unlimited and there are many convergences of form and physiol-
their branches. ogy among unrelated groups. We also find plants of radically different
Leaf shedders. appearances living side by side, an aspect that delights the eye and
makes them so fascinating.
to absorb water and exchange gases over all surfaces of submerged (a)
tissues. The permanently submerged species usually have the most
modified forms of gaseous exchange. In the majority of genera, the
aquatic leaves lack stomata altogether whereas in partly submerged
ones stomata are present only on the upper surface. The marine
species of Potamogetonaceae lack stomata, but have openings at leaf
apices.
Some bottom dwellers of cold oligotrophic lakes may have spe-
cial methods of carbon assimilation. They are small in stature with
highly compressed internodes, long cylindrical pointed leaves, and
relatively massive root systems. This suite of morphological charac-
ters has been termed ‘isoetid’. Carbon acquisition from sediment is
recorded for temperate species of Isoetes and other isoetids such as
Lobelia dortmanna and Littorella uniflora. Crassulacean acid metabolism
(CAM), which is usually characteristic of xerophytes and many epi-
phytes, has evolved in aquatic Isoetes as a response to daytime carbon
(b)
deficit. Apparently this plastic response is absent in terrestrial species
or lost in individuals stranded in drier habitats.
The other group of submerged aquatics that frequent cold olig-
otrophic lakes are also highly reduced in stature, but are quite dif-
ferent in morphology from the isoetids. They generally conform to a
Ceratophyllum type of body plan, for example the water-milfoil (Myrio-
phyllum alterniflorum), but include highly reduced examples of rushes
such as Juncus bulbosus and pondweeds such as Potamogeton filiformis.
Also ubiquitous in these cold-water lakes are the charalean algae,
Nitella and Chara.
The aquatic fern genus Azolla (Azollaceae) has a symbiotic relation-
ship with the bacterium (Anabaena azollae) that is capable of assim-
ilating atmospheric nitrogen. This alga lives in pits at the base of
the lobes. They have an increased surface area in relation to volume
because of the need to assimilate carbon dioxide directly from the
water. Oxygen, as a by-product of photosynthesis, is retained and
distributed by an elaborate aerating network (aerenchyma). In the (c)
and aid buoyancy. One of the fronds acts as a stabiliser and morpho-
logically resembles a root. Smallest of all flowering plants, the tiny
floating plants such as the duckweeds, Lemna spp. and Wolffia spp.,
rely entirely on dissolved nutrients to increase bouyancy. The sinking
and rising of the water-soldier, Stratiotes aloides, is noteworthy. Mostly,
it lives in calcium rich waters and, during the summer months, the
leaves gradually build up an encrustation of calcium carbonate. This
increases the specific gravity of the plant until it eventually sinks to
the bottom in the autumn. With the growth of fresh leaves in the
spring, the specific gravity of the plant lessens, and the plant rises to
the surface.
The actual shape of aquatic leaves appears to be directly influenced
by the physical properties of water, such as temperature, turbidity
and light transmission. The amount of light passing through water
drops dramatically, even after a few metres. Most aquatic leaves are
either long and ribbon-shaped, or are finely dissected, offering little
resistance to the flow of water. In floating leaves of genera such as
Nymphaea and Potamogeton, the cuticle is waxy, preventing waterlog-
ging and aiding runoff. Figure 6.6. Hottonia palustris
An abundant supply of water is the norm for many aquatic plants (water violet) has finely dissected
submerged leaves but produces an
but it may not be continually available. Many ponds and rivers are
aerial inflorescence on a long
drastically reduced in size during periods of drought or dry up com-
peduncle.
pletely. Cuticular development of the epidermis, and lignification of
the xylem of submerged leaves is highly reduced or absent. Like many
coastal seaweeds, fresh-water aquatic plants often have a covering of
mucilage and are slimy to the touch. This may retard excessive entry
of fresh-water into the plant tissues by osmosis, and subsequent loss
of assimilates, but it also may serve to prevent injury in flowing water,
or slow the process of dessication during periods of low water.
The rooted species have aerenchyma in the rhizomes and roots,
and normally have parts of the main axis submerged. Leaves and flow-
ers are either held above the water or floating on it. Such leaves fre-
quently have retrograde development of the palisade and parenchyma
layers and are relatively thin. However, they have a large surface area,
and tend towards a peltate shape that maximises light interception. In
the arrowheads, Sagittaria (Alismataceae), the aerial leaves are arrow-
shaped, whereas in most others they are oval to rounded, with the
petiole either angular to the plane of the lamina, or inserted cen-
trally. Most of them rely on water for some degree of mechanical
support, although the strongly ribbed leaves of Victoria amazonica can
support weights of up to 50 kg. The leaves of this genus also possess
folded margins up to 15 cm high. Water that may collect on the lam-
ina drains through minute pores. Long flexible petioles allow leaves
to float on the surface of still or slow-flowing water.
Leaves and petioles have well-developed aerating tissue or
aerenchyma. Many species in this group also possess submerged leaves
that are often finely divided and linear, for example the water-shields,
Cabomba spp. (Cabombaceae). In such cases, the cuticle is absent or
weakly developed and there are no stomata, thus increasing the
260 THE LIVES OF PLANTS
(a) achieve a more negative osmotic potential would be for the cells to
absorb salt to a higher concentration than seawater. This does not
happen because increasing salt levels would lead to the denaturation
of enzymes. For active metabolism of the cell, it is essential that the
cytoplasm remains free from excess salt.
When salt stress is due simply to deposition on foliage, as takes
place in foreshore habitats, cliffs and forward dune systems, most
plants attempt to resist the uptake of excessive amounts by means
of passive removal, or by various exclusion, and secretion processes.
As the degree of salt stress increases, such regulation mechanisms
(b) are inadequate, and other mechanisms such as succulence come into
prominence. The aquatic sea-grasses, and mangroves have the greatest
number of such adaptations. Dune and foreshore plants usually have
some resistance to salt spray, and possess some form of short term
avoidance of salt injury, or are annuals. Many have greater xerophytic
characteristics such as tough cuticles and sunken stomata. In contrast,
halophytic species of salt-marshes have few xerophytic adaptations,
(c) have thin cuticles, and stomata that are often more frequent and
unsunken. By transpiring freely, these plants make use of a large
throughput of water to alleviate exposure to high salt. Some, such as
Salicornia spp. (Chenopodiaceae), can also reduce the demands of the
shoots by absorbing rainwater directly through the cuticles.
Figure 6.12. Salt tolerance:
(a) thrift (Armeria maritima) in
flower; (b) transverse section of
6.3.2 Salt exclusion mechanisms
gland, a complex of 16 cells (from
Salt is excluded from the roots of many salt-tolerant species, includ-
Armeria); (c) proline molecular
structure.
ing Atriplex spp., but the salt exclusion mechanisms vary. Salt may
be excluded simply by the thick, tough epidermis, but tolerance to
moderate exposure usually relies on an endodermal barrier in the
roots. In salt-tolerant species of Puccinellia, the development of a dou-
ble endodermis retards the passage of salt into the xylem. Halophytes
such as Salicornia can separate fresh water from seawater by a simple,
non-metabolic ultrafiltration process combined with ion transport.
In some mangrove species salt is also excluded by ultra-filtration of
the endodermal layer of the root, driven by high xylem tension. This
results in a xylem sap that is almost pure water with an osmotic
potential of nearly zero.
In many species, particularly those of permanently saline environ-
ments, some form of active exclusion is usually present. Salt accumu-
lation in the shoots and leaves is prevented by an active transportation
of sodium ions from the roots that requires the expediture of energy.
Xylem parenchyma cells can function as ‘pumps’, which actively trans-
port sodium ions against the concentration gradient out of the xylem
via the symplast. Chloride ions are retained in the older parts of the
roots. Conversely, potassium, which is in low concentration in the
environment, is actively transported in. Carrier subunits of the root
Figure 6.13. Arthrocnemon, a membranes selectively bind to the ions and convey them across the
perennial relative of the glasswort
membrane, releasing them as free ions. The endodermis is cutinised
Salicornia.
and suberised, preventing re-entry of sodium.
6.3 HALOPHYTES 263
adopt this strategy are annuals, while others are perennials and annu-
ally shed leaves or die back in winter to a rhizome. At the end of
the growing season so much salt has accumulated in their tissues
that passive removal of salt by leaf shedding is a constant feature
of Juncus maritimus, J. gerardii, and other foreshore and salt-marsh
plants such as Limonium spp. Stem shedding also occurs in perennial
species of Salicornia. Senescence through salt accumulation in peren-
nials may account for the high number on annuals on foreshores.
On British coasts, the most common strandline and foreshore species
are all annuals, for example Salsola kali, Cakile maritima and Matricaria
maritima.
Other, more tolerant halophytes (both osmoregulators and osmo-
conformers), accumulate ions that are translocated to other parts of
the plant such as shoots and leaves. From there, it may be secreted
either by salt glands, through the cuticle, in guttation fluid, retrans-
ported through the phloem to the roots (Salicornia spp.), or else con-
centrated in special leaf hairs (Atriplex spp.). Salt-secreting osmoregu-
lators have a higher salt tolerance than those which don’t secrete.
Actively secreting families include the Chenopodiaceae, Tamari-
caceae, Frankeniaceae, Plumbaginaceae, Poaceae, Primulaceae, and
Convolvulaceae, etc., and mangrove families such as Rhizophoraceae,
Avicenniaceae and Acanthaceae, etc. Often such halophytes feel wet
or sticky to the touch. Salt glands which actively secrete salt are
found in the leaves, stems, or root cells of many genera such as
Limonium, Frankenia, Glaux, Spartina, and Tamarix. Salt gland cells lack
vacuoles and are rich in mitochondria. Usually, they are not accu-
mulating organs, but the saltbush, Atriplex, has two-celled hair-like
glands with a large bladder-like vacuole that ruptures to release
accumulated salt. The sunken leaf glands in Spartina anglica are also
hair-like.
Many halophytic plants, including mangroves, adjust their
osmotic potential by synthesising compounds in their cytoplasm that
can then exist at higher salt concentrations without denaturing the
enzymes essential for metabolic processes and maintain higher neg-
ative water potential in their xylem elements so that water is not
lost to the substrate via the roots by reverse osmosis. These compati-
ble solutes or ‘compatible osmotica’ such as proline (amino acid) and
betaines (methylated ammonium compounds) build up in the cells
and thus maintain a more negative osmotic potential, as a substi-
tute for salt. Plants that produce compatible solutes must not only
prevent the external salt from entering the cell but also prevent the
compatible solutes from leaking out.
The exact mechanism of compatible solute synthesis is not com-
pletely known, but it is linked to the degree of cell turgor and abscisic
acid (ABA). This has a general role as an endogenous growth regulator
and is involved in adaptation to water deficit stress. Many methylated
onium compounds are known to increase in response to salt stress, for
example betaines (Atriplex, Suaeda); related sulphonium compounds
(Spartina); proline (Aster, Mesembryanthemum, Salicornia, Triglochin);
6.3 HALOPHYTES 265
(a) (b)
6.3.4 Mangroves
Mangroves conjure up images of hot, impenetrable, mosquito-infested
swamps where walking is difficult and every step in the sticky mud
produces a stench of hydrogen sulphide and the way is barred by
stilt roots, but this is misleading. Many mangrove communities are
relatively open forests and may occur on rocky coasts. Mangroves are
mostly tropical trees that grow on exposed or submerged soils with
a high salt content in the inter-tidal zone, and from where the water
table is 50 cm or more beneath the soil surface to where the soil is
Figure 6.15. Pneumatophores
covered by 150 cm or more of water. In adjacent communities man-
are frequent and diverse. Aerial groves can penetrate extensively along river banks, while, in sheltered
roots hanging from branches estuaries and lagoons, they may form forests up to several kilometres
increase lenticel number. In wide. They are one of a number of usually discrete coastal communi-
Avicennia and Sonneratia they are ties, although many constituent species also occur in non-halophytic
finger-like or cone-like, simple and communities behind the mangroves. They comprise mainly rhizoma-
upright, and have chlorophyll in the tous perennials, and all produce aerial reproductive organs, but they
subsurface layers. Avicennia spp. are
have little or no capacity for vegetative regeneration. They belong to
pioneers of more sheltered areas,
a wide range of families, but there are really only four cosmopolitan
have great ecological amplitude,
and have facultative
mangrove families, for example the Rhizophoraceae, Sonneratiaceae,
pneumatophores. Sonneratia is Avicenniaceae and Combretaceae. There are some marginal genera
found on more or less exposed such as the palm Nypa (Arecaceae), which occasionally forms large
rocky or gravelly shores but also in stands of mangrove sub-types due to competitive exclusion of other
brackish water on deep mud. In species by rhizomatous habit (Figure 6.14). Mangroves often blend
Bruguiera the pneumatophores are into fresh-water swamps on the landward side, or to other shore-
knee-like projections. This genus line communities such as strandline vegetation, or marine sea-grass
prefers stiff clays of the inner
meadows.
mangrove, but it may be a pioneer
It has been hypothesised that mangroves are unlikely to have
along tidal rivers.
existed before the evolution of the seed habit, because the establish-
ment of free-living independent gametophytes may not have been
possible in seawater. There is a fossil leptosporangiate fern, Weichsella,
which is reputed to have formed extensive back-mangal communities
in the Early Cretaceous. Today, species of the fern genus Acrostichum
will tolerate some salt (Figure 6.17), but are generally to be found in
the back communities. It often grows on the mounds of the burrow-
ing lobster, Thalassina anabaena (Thalassinidae).
6.3 HALOPHYTES 267
(a) (b)
root from the soil, and root-hair development is suppressed. The fun-
gal mycelium penetrates between the epidermal cells and ramifies in
the inter-cellular spaces of the cortex. The network of hyphae in the
cortex does not penetrate past the epidermis and is called the Hartig
Net.
Endomycorrhizae involve a more intimate relationship between
fungus and host. Vesicular--arbuscular mycorrhizae (VA mycorrhizae)
are very widespread in many families including gymnosperms, ferns
and bryophytes, both in the tropics and temperate regions. The fungal
symbiont belongs to a single zygomycete family, the Endogonaceae.
Usually there is no fungal sheath. The fungal hypha flattens slightly
where it touches the root surface and then penetrates into or between
the epidermal cells. In the cortex the hyphae ramify between the cells
and vesicles are produced between the cortical cells, pushing them
apart to make space. Other hyphae penetrate the cell walls, producing
branched arbuscules surrounded by the plasmalemma or tonoplast.
The arbuscule, the site of nutrient exchange, is a transient structure
which eventually lyses.
The order Ericales (heathers, rhododendrons, blueberries, etc.)
often grow on acid soils that are very low in phosphate. They have
peculiar and varied mycorrhizae involving septate fungi. The fungal
symbiont, which provides the host with amnio acids, usually has
a wide tolerance of different ericaceous hosts in species-rich heath-
lands. Ericaceous mycorrhizae have been divided into two main types,
‘ericoid’ and ‘arbutoid’. Ericoid mycorrhizae are endomycorrhizal, and
are more common. Calluna produces thin ‘hair-roots’ that lack an
epidermis, and the single cortical cell-layer becomes heavily infected
with intra-cellular hyphal coils. More cortical cell-layers are present
(a)
in other genera. In arbutoid mycorrhizae, the fungus is symbiotic
with trees such as Arbutus, and is ectomycorrizal. A sheath and extra-
cellular haustoria are developed, but the Hartig Net is restricted to
the outer layers of the cortex and some cortical cells are also filled
with hyphal coils.
Many orchids have an obligate mycorrhiza. The tiny seeds can-
not germinate successfully in the absence of the fungus. A hypha
enters the seed through the suspensor region and penetrates the ger-
(b)
minating embryo. As the embryo grows, new infections are made.
The fungi are species of Rhizoctonia. There are two layers to the root:
an outer fungal host layer within which there is a digestion layer
where fungal hyphae penetrate and grow within cells. The hyphae
form intra-cellular coils or irregular structures called pelotons that
are digested by a process resembling phagocytosis, but repeated. In
orchids that die back to a stem-tuber, a new mycorrhiza is established
each season.
There are two main kinds of stem parasite: the large bushy aerial
hemi-parasites of trees, especially the mistletoes in the order Santa-
lales (families Loranthaceae, Viscaceae and Eremolepidaceae); and the
dodders Cassytha and Cuscuta. Stem parasites have some characteristics
of root parasites, in the development and form of the haustoria, which
links them to the host and in the reduced photosynthetic capacity
of some of them. Like root parasites, their host provides them with
water and nutrients. They have numerous stomata so that a high
transpiration pull draws water and nutrients from the host. How-
ever, it is possible that many stem parasites have evolved from and
share many features with ordinary epiphytes. Some epiphytes, such
as Aeschynanthus hildebrandtii (Gesneriaceae), have roots that penetrate
the bark of the host tree and are suspected of being at least partially
parasitic.
278 THE LIVES OF PLANTS
The distinction between stem and root parasite would seem fairly
arbitrary, except that different taxonomic groups have specialised in
either habit. This may indicate different evolutionary origins for each
kind of parasitism. The possibly greater specificity and wider taxo-
nomic distribution of root parasites is interesting. Root parasites may
have evolved either from direct root fusion or by sharing a mycor-
rhizal association, both of which require a close physiological com-
patibility, whereas stem parasites may have evolved from epiphytes
that generally do not have species-specific relationships.
The Santalaceae, which are related to the mistletoes, are particu-
larly interesting because they are root parasites, except for one genus
of stem parasite, Dendrotrophe. The Santalaceae are hemi-parasites with
no host preferences. Thesium has wandering roots that traverse the soil
at a depth of a few centimetres, establishing multiple contacts with
hosts, rather like the epicortical roots of the mistletoe Plicosepalus.
Perhaps the Santalaceae illustrate one example of the origin of stem
parasitism from root parasitism or vice versa.
Table 6.2 Types of plant traps (number of species in each genus given in
parentheses)
Pitfall traps have evolved in three orders of plants. Nepenthes spp. (a)
are climbers, often found in bogs or in areas of poor soils such as
peat-swamp forest. The pitcher develops from swelling at the end of a
tendril. In Darlingtonia and Sarracenia it forms from a folded/urcelate
leaf. The lid of the pitcher is a seductive device, has nectar secret-
ing glands on its inner surface, and is a rain-protecting canopy. The
rim is hard, round and glossy, with nectar-secreting glands within
the angles, and downward-pointing hairs. The water in the pitcher
may contain a wetting agent. Its pH is acid to neutral, but when food
is added it becomes acidic for the digestive enzymes to work. After
digestion it returns to neutral again. Digestive enzymes are ribonu-
cleases, lipases, esterases, acid phosphatases, proteases and possibly (b)
chitinase. The fauna of the pitcher includes ants, spiders, protozoans,
rotifers, crustaceans and fly larvae (including mosquitoes).
In Genlisea, which occurs on both palaeotropic and neotropic insel-
bergs, the prey is protozoa that are attracted by chemotaxis, the only
known example of this phenomenon in the plant kingdom. In Drosera,
the leaf surface has mucilaginous tentacles which are longest around
the leaf margins. They are only able to bend towards the leaf cen-
tre. The outer ones respond quicker and move more quickly than
inner ones. The glands are egg-shaped and reddish and have three
functions:
(c)
(1) to secrete mucilage and catch prey
(2) to secrete enzymes (peroxidase, acid phosphatase, esterase, pro-
tease)
(3) to absorb the resultant fluid into the plant’s system (assisted by
microscopic hairs on leaves)
(1) stalked sticky glands which catch and detain prey and secondarily
secrete globules of mucilaginous fluid
(2) stalkless glands with no mucilage, seated in a depression, digest
the prey
Figure 6.31. Pitcher plants
The leaves have no nectar but possess a slight scent. The presence of an showing convergence in different
insect stimulates the glands, which are mildly acidic. The main supply families: (a) Nepenthes
of enzymes is from the stalkless glands. The enzymes are ribonucle- (Nepenthaceae); (b) Sarracenia and
ase, esterase, acid phosphatase, amylase and protease. The secretion (c) Darlingtonia (Sarracenniaceae);
and (d) Cephalotus
contains a mild bacteriocide to prevent infection from undigested
(Cephalotaceae).
prey.
282 THE LIVES OF PLANTS
The name epiphyte is derived from Greek, the prefix ‘epi-’ means
(c) ‘upon’. An epiphyte is a plant that grows upon another plant. Epi-
phytes are not parasites and do not directly obtain nutrition from
the host tree upon which they grow, although they can be said to
harm the host indirectly. They are not innocuous hitchhikers, and
heavily infested trees often show signs of morbidity or injury. Trees
in a senescent state tend to be prone to epiphyte infestation. Since
epiphytes live in an environment dominated by fluctuating nutrient,
moisture and light levels, they can be said to be adapted to with-
stand periodic stresses. The means of procuring mineral nutrients and
moisture are crucial to an epiphyte and can impact on other organ-
isms within its sphere of influence. In many mature forests epiphyte
load is greater than that of understorey herbs and not infrequently
Figure 6.39. Colour patterning
the collective leaf surface areas of epiphytes exceeds that of the host
of leaves of shade plants:
(a) Acanthaceae; (b) Maranta
tree.
(Marantaceae); (c) many plants of Epiphytes are characteristic of tropical forests, oceanic islands,
shady habitats have a purple etc., where there is year-round high energy levels and high humid-
underleaf that back scatters light ity. There is a decrease in vascular epiphytes with increasing latitude.
into the leaf. They occur also in temperate forests of New Zealand, Tasmania, South
America and the monsoon regions of the Himalayas where the macro-
epiphytes are mostly ferns. This asymmetry of distribution is due to
mesic conditions and a more or less oceanic climate in the South-
ern Hemisphere. Only four macro-epiphytes occur north of Florida in
North America, and perhaps only the fern Polypodium in the British
Isles. At high latitudes where winter light levels are low and where
winter drought and frost, particularly air-frosts, are severe, flower-
ing plants are at a disadvantage, especially for the critical stage of
establishment. Frost allows survival of only micro-epiphytes such as
bryophytes and lichens.
6.6 EPIPHYTES, HEMI-EPIPHYTES AND VINES 287
There are about 900 genera and almost 30 000 species of epiphytes (a)
in the world, but there are no totally epiphytic families. In most plant
families epiphytes are insignificant, a spectacular exception being
the Orchidaceae. There are between 20 000 and 25 000 orchids in the
world and two out of three (70%) of them are epiphytic. Some 44% of
all vascular plant orders and 16% (or about 65 families, 11 of which
are ferns) of all vascular plant families have epiphytic species, but
only 32 seed plant families have five or more. About 20% of the pteri-
dophytes are epiphytic. There are about 143 species of Lycopodium that
are epiphytic while only five species of Selaginella are epiphytic. Gym-
nosperms are rarely epiphytic and this is consistent with their slow (b)
maturation, massive axes, anemophily and heavy seeds.
There are slightly more families with epiphytes in the Palaeotrop-
ics than in the Neotropics (43:42), and there are six times more epi-
phytes in Central and South America than in Africa.
Speciation of epiphytes is greatest in the Neotropics; the num-
bers of cacti and bromeliads account for this. Africa, with about
2400 epiphytes, and only about 50% of the families found in other
Palaeotropical areas is poorest. This was probably because of impover-
ishment during dry periods of the Pleistocene. Australasia is impov-
erished compared with the Americas (10 200 compared with 15 500).
These distributions and diversities are the result of historical accident.
Each continent has evolved its epiphytic flora independently from
terrestrial relatives (sometmes several times over); for example most
epiphytic Neotropical orchids belong to the subtribes Maxillarinae,
Oncidinae and Pleurothallidinae, whereas the epiphytic Palaeotrop-
ical orchids belong to the subtribes Dendrobiinae and Bulbophylli- Figure 6.40. Epiphytic orchids:
nae. The Palaeotropics are richer in ferns, Araceae and Asclepiadaceae (a) pendulous orchid in flower;
while Australasia is better represented by Rubiaceae (see Figure 6.41). (b) pseudo-bulbs.
(a) (b)
Figure 6.41. Epiphytes with a rosette form trap detritus and water: (a) epiphytic
bromeliads in neotropical forest; (b) bird’s nest fern (Asplenium).
288 THE LIVES OF PLANTS
(a) (b)
(a)
pressure thereby encouraging the flow of water back into them. The
parenchyma also provides relatively unspecialised cells, which may
allow regeneration of the vascular tissue through the formation of
successive cambia, or after wounding.
There is distinct stratification among bole climbers. Top layers are
distinctly photophytic, for example Freycinetia (Pandanaceae). Below
this are mixed groups of aroids (Araceae), Gesneriaceae and Ericaceae,
which are themselves stratified. Below this again are the sciophytic
ferns. Most are shade-loving woody or suffrutescent perennials and
don’t display many obvious adaptations apart from aerial roots, but a
few are succulent, for example Cactaceae and some Piperaceae. Many
have increased amounts of chlorophyll or special pigmentation (see
Section 6.3), and have varying degrees of dorsiventrality. Many start
life in the soil but later lose contact with it as they root to the support
tree. In areas with lots of sunlight (gaps, etc.) the climbers are often
scrambling herbs.
(b)
6.6.2 Stranglers
Primary hemi-epiphytes such as stranglers (Ficus, Schefflera, Fagraea,
etc.) start as holo-epiphytes in the crowns of young trees, and are
carried upwards with the replacement canopy. They may have crowns
larger than the host crown, which may show considerable loss of
photosynthate through crown competition. Stranglers can maintain
Figure 6.45. Woody lianes have
a specialised xylem. (a) Crinkly their large canopy because they send their roots, which are often
lianes have flexibility; (b) dimorphic free-hanging, to the soil. The roots increase in number and girth and
vessel elements, broad ones for eventually self-graft or anastomose so that they eventually encircle
water conduction, narrow ones the host tree and ‘strangle’ it (Figure 6.46). Most grow in clearings,
for safety. forest fringes and gaps.
cycle used by soil rooted perennials. In this way they retrieve nutrients
lost from the above-ground parts (for example, through leaching and
leaf drop), and intercept water and atmospheric inputs, which would
otherwise be accessible to their host.
Their low productivity and substantial powers of nutrient-
accretion increase their impact on biogeochemical cycling. They are
thus major participants in the movement of mineral nutrients within
tropical forests. Attempts to analyse the structure and function of
tropical forest ecosystems cannot be wholly successful until epi-
phytes are given due consideration. Apart from anchorage in trees,
there is no common factor of growth form, seed type, pollen vec-
tor, water/carbon balance, source of nutrient ions or resource pro-
curement mode. Therefore, the life-form concept of ‘epiphyte’ must
include a greater diversity of more subtle variation. Species inhab-
iting the same area of forest and the same tree crown may differ
in their light and humidity requirements. Many orchids, including
closely related species, form assemblages on the same host, prefer- (a)
ring similar bark qualities, humidity and exposure.
Open-crowned, slow-growing trees with absorbent stable bark
make the best hosts. Epiphytes are generally commoner where tree
canopies are humid for most of the year, for example in swamp
forests and other humid situations such as enclosed valleys. Mois-
ture is probably the most important criterion of all. Temporal access
to moisture, avoiding drought injury, is the most immediate chal-
lenge, and year-round, high atmospheric humidity rather than high
total rainfall is most conducive. Epiphyte diversity is greatest in wet (b)
through a forest with some regularity but its movements are rapid
and it leaves little residue. Stem flow and through-fall are usually
dilute. Atmospheric inputs may be very uneven and almost every
canopy may be characterised by frequent or prolonged intervals of
extreme deprivation. Leachates may be important in breaking seed
dormancy. Some orchids may be confined to trees that can support
mycorrhizal fungi.
Perhaps the best way to begin analyses of epiphytes is to consider
the forest to be analogous to the oceans. At the top there is a photo-
synthetic layer (euphotic zone) where most of the production occurs.
This is the canopy. Below the canopy, in the shade zone (oligophotic
zone), photosynthesis decreases along with diversity until we reach
the bottom layers where there are only specialist scavengers that
feed on the detritus falling down. The fluctuating boundary between
the two is called the ‘morphological inversion surface’ or MIS. Above
this there are air-movement, moisture and temperature fluctuations;
below this there are stillness and uniformity. The MIS also effectively
defines the holding level for understorey and juvenile trees.
Epiphytes may also be classified by their means of obtaining
water, for example many that are ‘continuously supplied’ (CS) occur
within the shade zone and are mostly ferns or aroids. Some have
CAM (not aroids) while in others the velamen of the roots is not so
developed. Many trap organic detritus by means of ‘trash baskets’,
or have mycorrhizal associations and a prolonged life cycle. In con-
trast, other epiphytes which are ‘pulse-supplied’ (PS) are found in the
sun zone. The PS epiphytes usually have CAM, a reduction in surface
area:volume ratio, and a telescoping of parts (e.g. orchids, bromeliads
and cacti). Many possess velamen on their roots, absorbing trichomes,
etc., and absorb moisture from the atmosphere. The PS epiphytes are
often ant-plants (myrmecotrophs) while many also have mycorrhizal
associations.
Carbon fixation by means of crassulacean acid metabolism (CAM)
is widespread in canopy epiphytes although this phenomenon is most
frequently found in plants of arid climates. Canopy epiphytes usually
also possess succulence, low surface area:volume ratios and low tran-
spiration rates. They usually lack a well-developed palisade layer and
most of the photosynthetic cells are spongy mesophyll. CAM is present
in 26 flowering plant families. CAM plants, like all plants, must obtain
water and CO2 but if they fully open their stomata during daylight
they transpire too much water. They therefore open their stomata at
night only and fix CO2 into malic acid by the enzyme PEP carboxylase.
Malic acid is stored in the vacuole. Starch is degraded by glycolysis
to PEP. HCO− 3 reacts with PEP to form oxaloacetate, which is then
reduced to malic acid by the enzyme malate dehydrogenase. Malic
acid disappears during the day. It diffuses out of the vacuole and is
decarboxylated with the release of CO2 . This CO2 is then utilised by
the plant in daylight via the Calvin cycle of photosynthesis. Often
CAM plants are facultative C3 and can switch to this mode in cloudy
weather or following rainstorms.
6.6 EPIPHYTES, HEMI-EPIPHYTES AND VINES 293
(a) between ‘wet active’ and ‘dry inactive’ and a few are ‘resurrection
plants’ with an ability to ‘rebound’ rapidly, although poikilohydry in
epiphytes is found only in areas where moisture is abundant. Most
epiphytes are homoiohydric (avoid dessication).
Because of the patchiness of suitable microsites (as a result of
both the dispersion of host trees within the forest and the separation
of their branches), there is often a scarcity of conspecifics and so
aerial dispersal is the most frequent mode of spread (i.e. zoophilous
pollination and wind-dispersed seeds). Usually the seeds are tiny and
lack appendages (but see Aeschynanthus spp.: Gesnericeae).
Monocots (about 25% of all flowering plants) have five times the
number of epiphytic species (especially in the families Orchidaceae,
(b) Bromeliaceae and Araceae) in comparison with the rest of the flow-
ering plants, and twice the number with fern epiphytes. However,
there is no common monocot adaptive theme, although they possess
many features that appear to confer advantages as epiphytes. Most
species are iteroparous, with a rhizomatous, sympodial habit, and
serial perennation with determinate offshoots. Each ‘phyton’ is rela-
tively autonomous with leaf, associated adventitious roots, buds and
subtending stem segment. The meristems receive fixed carbon, mainly
from nearby leaves (i.e. there is reduced translocation over the whole
(c) plant). The reticulate stele gives greater capacity for functional inte-
gration and extensive vegetative renewal with a minimum of tissue
space. The meristematic regions remain as nutrient sinks whereas in
times of stress dicots will self-prune by aborting leaves, branches and
flowers.
Orchids have an affinity for acidic, humic, infertile soils (i.e. with
reduced nitrogen), and utilise NH4 rather than oxidised nitrogen,
and this may have predisposed them to epiphytism since mycorrhizae
mobilise nitrogen and phosphorus from sterile soil. Epiphytes, espe-
cially impounding ones, increase canopy humidity, which makes it
more favourable for nitrogen-fixation. Many orchids have extensive
Figure 6.49. Tillandsia nitrogen-fixing epiphyllae (which in turn have a symbiotic relation-
(Bromeliaceae), the genus of ship with Nostoc, a blue-green alga). Epiphytes may be more important
air-plants, has two main forms:
to the forest fauna than their numbers and biomass would suggest.
(a) upright rosettes and
Epiphytosis causes treefall and an increase in the physiognomic diver-
(b) pendulous. Bromeliad leaves
absorb water through scale-like sity of the forest, especially montane forest.
trichomes, as shown in (c). Bryophytes are most important in the water balance of tropical
montane forests and the dynamics of their vascular plant associa-
tions (Figure 6.50). By intercepting more than 25% of precipitation
they control and impede drainage, and can thus influence climate
on a local scale. Many species, especially epiphylls in tropical forests,
are associated with blue-green algae and fix atmospheric nitrogen.
This is the main input for nitrogen in tropical rainforests. As with
other epiphytes, bryophytes can profoundly alter the physiognomy
of forests due to ‘epiphyte load’ and consequently affect biodiversity.
When wet, mosses can be up to four times their live weight. The epi-
phyte biomass and interceptive capacity are proportional to annual
rainfall where the monthly average is more than 100 mm, whereas
6.7 GRASSLANDS AND SAVANNAS 295
6.7.1 Grasses
The widespread occurrence and predominance of grasses in the vari-
ous types of world vegetation results from:
r adaptation to a range of soil types
r adaptation to a diversity of climates and a broad ecological ampli-
tude
r ability to compete successfully with other plant types
r ability to survive high levels of predation
296 THE LIVES OF PLANTS
All green plants utilise ribulose diphosphate for the initial cap-
ture of carbon dioxide from the atmosphere. Many grasses, how-
ever, possess an additional chemical pathway that utilises the three-
carbon compound phosphoenol pyruvate (PEP). This is known as the
Hatch/Slack or C4 pathway. This pathway is possible because of its spa-
tial separation in the leaf-blade anatomy (Kranz anatomy) from the
Calvin cycle. In grasses without this extra pathway (i.e. those with
only a C3 pathway) the Calvin cycle alone, operates in the diffusely
arranged cells of the chlorenchyma. The Hatch/Slack pathway oper-
ates in the radially arranged cells of the chlorenchyma and releases
carbon dioxide into the outer bundle sheaths, where it is incorpo-
rated into the Calvin cycle. Plants with the Hatch/Slack pathway have
a much higher rate of carbon dioxide uptake and higher growth rates
than those in which it is absent. The C4 pathway reduces photores-
piration. Because it operates most efficiently in high temperatures
and high light intensities it occurs widely in tropical grasses such
as Andropogon, Panicum and Eragrostis. Temperate grasses such as Poa,
Bromus and Festuca gain no advantage from this extra pathway so they
retain the Calvin cycle alone.
Most grasses have stems that are hollow, easily bent and yield to
the wind. Stems do not increase their size by growing thicker at the
sides and longer at the top. The thickness is fixed from the beginning,
and the stem increases by the meristematic region (intercalary) at the
base just above each node. The intercalary meristem is protected by
sheathing leaf bases. Grasses do not develop taproots, and the adven-
titious roots are slender, relatively short, with infrequent branching.
They originate in large numbers from the base of the plant (e.g. Fes-
tuca). Alternatively, the roots may be few and very long, extending
deeply in the soil or remaining near the surface (e.g. Aristida pungens).
Grasses with such roots are able to utilise all available surface water.
Many grasses, especially perennials, have horizontal underground
rhizomes (e.g. Agropyron) or overground stolons (e.g. Cynodon), and
produce new plants at intervals along their length. Rhizomes are
Figure 6.51. One of the more often tough and serve to anchor the plant in the soil, as well as
familiar grasses, Cortaderia selloana to colonise new ground (e.g. marram grass, Ammophila arenaria; rice
(pampas grass). Grasses are mostly grass, Spartina townsendii) (see Figure 6.52).
small tufted plants, but Grasses do not develop a permanent main stem with side branches
occasionally may, like pampas (except bamboos). They grow from a basal rootstock, and the leaves,
grass, form large robust tussocks which are simple, often die back at the end of each season in peren-
with a stout central axis composed
nial species. They are therefore mostly small tufted plants, but occa-
of tightly packed dead leaf bases.
sionally may be large, forming robust tussocks with a stout central
6.7 GRASSLANDS AND SAVANNAS 297
axis composed of tightly packed dead leaf bases (e.g. pampas grass,
Cortaderia selloana). In tropical regions of seasonal or low rainfall there
is often a danger of fire started by lightning or by humans. Grasses
are able to survive because new growth is initiated at the rootstock
below ground level. Tropical savanna grasses such as Andropogon and
Saccharum, and the giant reed Arundo donax, may have stems exceed-
ing 3 m. The leaves are borne in two ranks at intervals along the stem.
They originate from nodes and comprise a basal sheath clasping the
stem, and a blade which is usually narrow and flat, folded or rolled. Figure 6.53. Bamboo is rich in
hard fibres, giving the the hollow
Just above each node is the intercalary meristem. Differential growth
stems great strength.
of this meristem allows grasses to bend upright after trampling. Leaf
blades also grow by a basal meristem situated at the junction with
the sheath, permitting the blade to grow despite the removal of distal
parts by grazing. At its upper end, the sheath passes into a parallel-
veined blade. The blade is typically long and narrow but may be broad
in shade-loving species. At the junction of sheath and blade is a short
membranous rim, called a ligule, that may prevent rain entering the
sheath.
Grasses only need a piece of stem bearing leaves with node and
internode in order to reproduce vegetatively. Adventitious roots read-
ily grow from a node, while new shoots grow from buds in the axils
of the leaves. This is the way that grass cover and sugarcane is estab-
lished in horticulture and agriculture, respectively (i.e. by ‘seeding’).
In many tufted or tussock species vegetative growth is by tillering.
New shoots grow out from the leaf axils at the base of the plant,
to form a rosette or tussock (Figure 6.54). Other grasses may spread
by stolons, stems that grow from the base of the mother plant and
spread horizontally over the surface of the soil, producing a new
plant at each node. This method is common in tropical grasses such
as Bermuda grass (Cynodon dactylon). In temperate grasses a similar
effect is achieved by rhizomes (under the soil surface). It has been esti-
Figure 6.54. Tussock grassland
mated that a single plant of Festuca rubra, which spreads by rhizomes,
in New Zealand.
may be some 250 m (>800 ft) in diameter and up to 400 years old,
298 THE LIVES OF PLANTS
(a)
(b)
and the fever tree (Acacia) in Africa. Some plants with very succu-
lent or swollen stems may have normal leaves; for example, Pachy-
podium (Apocynaceae) from Madagascar; Adenium (Apocynaceae) from
northeast Africa, Vitex from South Africa, and even the baobabs and
their relatives (Sterculiaceae) from Africa and Australia. The boojum
(Idria columnanis: Fouquieriaceae) from Mexico is another such plant
(Figure 6.61).
New Caledonia is the most distinct of the Pacific islands, and has
a unique flora that is totally distinct from other forests of Melane-
sia. The 75% endemism of the forest flora is the result of the long
isolation and great age of the island, as well as the general preva-
lence of ultrabasic rocks. These factors have influenced the mon-
tane flora of New Caledonia no less than the lowland vegetation. The
commonest tree ferns on ultrabasic soils are Dicksonia spp., whereas
Cyathea spp. are on schists. Endemic families of the New Caledonian
montane forests include Paracryphiaceae (Paracryphia), and Strasburg-
eriaceae (Strasburgeria). Unique endemic genera include Apiopetalum
(Araliaceae), and Canacomyrica (Myricaceae). Among the conifers there
are five endemic species of Agathis and twelve endemic species of Arau-
caria, plus the endemic genera Neocallitropsis and Libocedrus (Cupres- Groups that show extreme
saceae), and Austrotaxus (Taxaceae). The latter is an isolated member disjunction, on the
of the essentially Northern Hemisphere yew family. It reaches heights Mascarene Islands and
of about 25 m, but it is rather rare, growing at relatively low eleva- Hawaii include:
tions from 600 to 800 m. Astelia, Dianella (Liliaceae s.l.),
If we look at the extinction and localisation of floras on large Cordyline (Lomandraceae), Pipturus
land masses such as North America or Australia we see that it is pre- (Urticaceae), Peperomia
cisely older elements such as conifers and woody flowering plants (Peperomiaceae),
that are also restricted to narrow and declining ranges, for example Diospyros (Ebenaceae), Myrsine
Agathis, Araucaria (Araucariaceae), Nothofagus (Fagaceae), Fremontoden- (Myrsinaceae), Canthium,
Psychotria (Rubiaceae),
dron (Sterculiaceae), Franklinia (Theaceae), and Lyonothamnus (Rosaceae).
Pittosporum (Pittosporaceae),
Lyonothamnus, now confined to offshore islands of California, is very
Elaeocarpus (Elaeocarpaceae),
closely related to the genus Vauquelinia that has about nine species Zanthoxylum (Rutaceae).
extant in the Sierra Madre ranges of Mexico where one species extends
to the Big Bend region of Texas. The recent discovery of a new genus
(Wollemia) of the Araucariaceae in a relatively well-explored part of
Australia clearly shows how radically different the floras of the past
must have been.
distributed from the Nicobar Islands to the Marquesas and is the most
widely distributed genus of its family. Across its range it has speci-
ated greatly on many islands such as Borneo and New Guinea, but
it is on Hawaii that it has undergone the most explosive speciation.
Metrosideros (Myrtaceae) is another genus with species that are found
on all the major islands of the Pacific, while Hebe (Scrophulariaceae),
in New Zealand is another classical example.
Many island plants have evolved in isolation from a single invasion
event. The gene pool of the original coloniser was only a small fraction
of the total gene pool of the species. The effect of selection on this
limited gene pool is known as the founder effect and is the mech-
anism postulated for the evolution of bizarre giant herbs of many
islands. We expect rapid evolution on islands to be aided by lack
Figure 6.71. Aeschynanthus.
of predators and competitors, a wide spectrum of ecological oppor-
tunities and isolating mechanisms, but the ability to evolve also
depends on the genetic makeup of each particular plant group. The
effects of small mutations on developmental programmes, and of
pleiotropic genes, can cause massive shifts in morphological and eco-
logical parameters. Polynesian lowland forests contain woody groups
that are herbaceous on continental mainlands, for example Lobeli-
aceae, Asteraceae, Amaranthaceae. Not all plant families have devel-
oped arborescence. For example the genus Viola (Violaceae) on Hawaii
is herbaceous or woody but does not form ‘trees’. This is in marked
contrast to the lobelioids (Lobeliaceae) and silversword alliance (Aster-
aceae) that have radiated into diverse arborescent forms.
‘death wish’ and prove difficult to maintain for any length of time.
In the wild a paucity of individuals also plays a key role in loss
of genetic variability. When loss of variability occurs, potential for
change is halted. Some of these vanishing genera that show this
unfortunate tendency include Nesocodon, Heterochaenia and Musschia
(Campanulaceae); Delissea, Brighamia, Rollandia, Cyanea and Clermontia
(Lobeliaceae); Hesperomannia and Romya (Asteraceae); Hibiscadelphus and
Kokia (Malvaceae); Trochetiopsis (Sterculiaceae); and Pteralyxia (Apocy-
naceae).
But lo! men have become the tools of their tools. The
man who independently plucked the fruits when he was
hungry is become a farmer; and he stood under a tree
for shelter, a housekeeper.
Henry David Thoreau, 1817–1862
has been the selection of varieties that are able to make use of the
high levels of fertilisers. Cultivars have become adapted to different
climatic regimes and different photoperiods (that is, day lengths in
different latitudes).
Crop plants have faced less competition, while irrigation and
the the application of fertilisers have minimised stress. A rapid or
annual life cycle has been selected. Seeds and tubers lacking dor-
mancy and with rapid and uniform germination, or clonal repro-
duction at the expense of sexual reproduction have been selected.
Synchronous development and ripening has been selected to enable
more efficient harvesting.
Plants are a source of food and pleasure and material for construc-
tion. The same species can provide all three. Many crop species were
initially domesticated for one purpose and then a different part of
the plant was exploited. The brassicas are an outstanding example
of a kind of plant in which almost all parts of the plant have been
exploited in one way or another. Brassica oleracea, B. campestris, and B.
napus are closely related species that exist as an astonishing range of Table 7.1 Brassicaceae
crops. cultivated for food
Two particular kinds of plants, the bamboos and the palms, are
the supreme champions for the number of different uses they have. Cabbage
Cauliflower
There are supposed to be over 1000 uses of bamboo. There are more Kales
than 40 different genera of bamboo and hundreds of species. Many Mustards
Chinese brassicas
grow to great heights; up to 37 m has been recorded even though wong nga baak
bamboo is an herbaceous species. There is a branched rhizome from baak choi
which the culms expand very rapidly like the sections of a telescope; hoi sum, etc.
Broccolis
growth of nearly 1 m per day has been recorded. So important is Turnips
bamboo that it holds a central place in Chinese and Japanese art Swedes
and mythology. The first monograph on any plant group was ChubPhu Kohlrabi
Sarson
written by Tai Khai-Chih about ad 460. Bamboo is said to combine Oilseed rapes
the strength of steel with great lightness. The strength and lightness
comes from the hollow tubular structure with fibres around its mar-
gin. The hollowness has been utilised as pipes even for piping natural
gas. The elasticity of the fibres is a great advantage in regions of hur-
ricanes. The exterior has a thick waxy and silicon-impregnated coat
that is highly resistant to the weather and to pests and diseases.
Palms do not just provide coconuts. There are nearly 3000 species
of palm. They provide drink, seed, fruit, timber, and fibre. Even just
from the coconut (Cocos nucifera) alone there is drink, a food and a
fibre. The borassus palm (Borassus flabellifer) (Figure 7.1) has 801 uses
according to a Tamil song. Palm wine is produced by tapping the
immature male inflorescence in several other species including Elaeis
guineensis (Figure 7.2) and Nypa fruiticans, the mangrove plam.
Date palms, Phoenix dactylifera, provide large quantities of fruit
with yields often in excess of 30 kg per tree. Favoured trees have been
propagated from vegetative suckers for millennia. Phoenix dactylifera
is dioecious and wind-pollinated but it was early understood that the
amount of fruit set could be enhanced by pollination by hand. Today
320 THE FRUITS OF THE EARTH
Europe has been mapped, reaching Britain 5000 years ago. Cultivars
arose that were adapted to different daylength (or were day-neutral),
seasonality, rainfall and temperature and different soils.
The first domestication of rice occurred a little later than wheat.
Pottery shards bearing the imprint of both grains and husks of Oryza
sativa were discovered at Non Nok Tha in the Korat area of Thailand
dating from 6000 years ago. The spread of rice from its proposed area
of domestication in northern Thailand, Myanmar (Burma), Assam or
southwestern China northwards into China depended to some extent
on changes in agricultural practice. Puddling of soils extended soil
moisture availability. Transplanting of seedlings 1--6 weeks old in pad-
dies gave rice plants a start over other plants and increased yield.
Elsewhere rice remained an upland dryland crop. Only later was wet-
land cultivation spread by the migration of peoples to other areas
in southeastern Asia. Wetland cultivation is so extensive now that
methane-producing bacteria in ricefields are suspected of putting
115 Mt of methane, equivalent to all the world’s natural swamplands,
into the atmosphere each year adding to global warming.
7.2 PLANTS FOR FOOD 323
It was the introduction of new cultivars of rice that was one of the
key aspects of the so-called green revolution of the 1960s. The new
varieties had a shorter stature with a greater allocation of energy
to the grain rather than leaf, and higher responsiveness to nitrogen-
based fertilisers. The new varieties (one particularly successful one
was called IR8), had the potential for much greater yield and were
day-neutral, so they could be grown at any latitude. At the same time
new varieties of wheat enabled the enhanced cultivation of wheat in
drier areas such as Pakistan and Mexico.
However, there were negative consequences. Some of the new vari-
eties were disliked because of aspects that had not been identified in
the breeding programme, for example IR8 was disliked for its cook-
ing quality. Some new wheat varieties were red rather than amber in
colour. Perhaps, more importantly, there was a loss of genetic diver-
sity as long-cultivated land races were abandoned. The new varieties
were actually part of a package that included new methods of cul-
tivation. Although yields were greater so were inputs, especially in
fertiliser.
The early history of maize (Zea mays) is obscure. It is related to
teosinte Zea mexicana, a weedy annual. Teosinte looks, at least super-
ficially, very different, so different that for many years it was placed
in its own genus called Euchlaena.
Maize and teosinte are diclinous, having separate male and female
inflorescences on the same plant. Maize and teosinte differ especially
in the form of the female inflorescence (Figure 7.4). The origin of
maize may have been by transmogrification of the corn so that each
lateral branch was shortened and the terminal male tassel feminised.
In maize, like rice and wheat, there has been very extensive diversi-
fication of cultivars. Three major types of maize are grown; grain or
field corn, sweetcorn and popcorn. Grain or field corn is by far the
main kind; 70% is fed to animals and more used as silage. It is clas-
sified into four main types; Dent, Flint, Flour and Waxy, which differ
in the distribution and type of starch in the kernel.
324 THE FRUITS OF THE EARTH
Field Dent Hard starch at the sides and a soft type in the centre of kernel, but shrinking at
apex on drying to produce a dent (starch = 30% amylose, 70% amylopectin)
Flint Hard starch layer entirely surrounding the outer part of the kernel (30% amylose,
70% amylopectin
Flour Very thin layer of hard starch and almost entirely soft starch (30% amylose, 70%
amylopectin)
Waxy Starch consists almost entirely of amylopectin
Nearly all the maize grown in the USA and Canada is hybrid corn
produced by crossing inbred lines. Crosses are ensured by detasseling
(i.e. emasculating one line) or by the manipulation of male sterility
genes. The utilisation of a particular sterility genotype exposed maize
to attack by the mildew Helmonthosporum maydis.
Within the regions once covered by savanna grasslands a range
of other cereals are grown; sorghum and various kinds of millets.
Sorghum is the staple food for 500 million people in 30 countries in
Africa, India and China. It matures in as little as 75 days and is highly
photosynthetically efficient. It can grow in both temperate and tropi-
cal conditions but is especially favoured in tropical conditions where
maize cultivation is marginal because of drought, salt and water-
logging. It is utilised in various ways; boiled like rice, cracked like
oats for porridge, malted like barley for beer, baked into flatbreads,
popped for snacks, or eaten green like sweetcorn. However, it has a
high tannin content that depresses nutrient absorption and a large
quantity of protein content is the poorly absorbed prolamine. There
are several different types of Sorghum arundinaceum including durra
(the main grain in Africa), milo (the main grain in Central America),
kaolang (grown in China) and feterita, which has large red-yellow or
white grains.
Pearl millet (Pennisetum glaucum) has a relatively low yield but is
more adapted to heat and drought than maize, and it is more nutri-
tious than sorghum. Steam cooked, it is known as couscous, but it
is also used to make breads, fermented foods and porridges. Finger
millet (Eleusine coracana) is a useful grain because it is rich in the
amino acid methionine lacking in the other tropical staples such as
cassava and plantain. It is a demanding crop requiring intensive cul-
tivation at weeding and harvesting stages. Fonio (Acha or white fonio)
Digitaria exilis and Digitaria iburua (black fonio) are two more kinds of
millet grown in the West African savanna region. Fonio is favoured
because of its taste and is rich in methionine and cysteine, normally
deficient in grains. It matures very rapidly, in as little as 6--8 weeks
after sowing.
Grasslands are also very important as pasture for domesticated
animals, especially cattle and sheep, and are also cultivated as fodder
7.2 PLANTS FOR FOOD 325
crops or for silage. Some pure grasslands of maize are cultivated but
mixed grasslands, generally dominated by Festuca (Fescues) or Lolium
(perennial ryegrass), are the most important sources of fodder. Usually
they are improved by mixture with legumes, like alfalfa and clover,
which, because of their nitrogen fixing-abilities, produce a fodder or
silage with higher protein content. Legumes are sometimes sown sep-
arately for fodder and various kinds of leafy vegetables (beet, swedes,
carrots) are also sometimes used. In drier areas grassy sorghums,
including Sudan grass (Sorghum sudanense), are widely grown as fodder
and pasture.
There are a few other species that have been harvested as grains
but are not grasses, especially from the family Polygonaceae. They
were important in Neolithic cultures and have been important famine
food. Buckwheat (Fagopyrum esculentum and F. tataricum) is the most,
important, with a reported harvested area of 2 582 589 ha worldwide.
Used mainly as food for poultry, buckwheat also provides a kind of
flour useful for gluten-free diets. It is also used in the Far East to make
noodles. Bees make a dark, highly flavoured honey from the pollen
and nectar. Quinoa (Chenopodium quinoa) is a similar ‘grain’ popular
especially with health-food enthusiats.
7.2.2 Pulses
The pulses are all legumes from the family Fabaceae (or Leguminosae).
There are many different species. They are especially important as
food not only because they are two to three times richer in protein
than cereals, but also because the spectrum of proteins they contain
is different from cereals. They are especially important as a source
of protein for poorer people in the tropics. Soybeans (Glycine max) are
said to contain all the essential amino acids in a quantity sufficient
for an adult. Legumes are generally rich in lysine, which is in low con-
centration in cereal protein, but they are generally low in methionine
and cysteine.
The range of proteins in pulses is very great though this can cause
dietary problems. Peanut allergy, mainly to a number of low molec-
ular weight proteins in peanuts, has become a serious problem in
the west in recent decades. The potential dangers for some people of
eating faba or broad beans (Vicia faba) have been known for many mil-
Table 7.4 Legume crops
lennia in the Mediterranean region; some classical authors advised
against eating them. A large minority of people in this region have Soybeans Glycine max
favism, an allergic sensitivity to eating the beans or even inhaling Beans Phaseolus vulgaris
Groundnuts Arachis hypogea
their pollen, causing haemolytic anaemia. People with favism have a Chick-Peas Cicer arietinum
form of genetic deficiency in an enzyme called glucose-6-phosphate Cow Peas Vigna unguiculata
Peas Pisum sativum
dehydrogenase (G-6-PD). This is the commonest human enzyme defi- Pigeon Peas Cajanus cajan
ciency and its distribution is associated with the distribution of Lentils Lens culinaris
malaria in past times, because it confers some protection against Broad Beans Vicia faba
Vetches Vicia species
malaria. Lupins Lupinus albus,
Lentils, peas, vetches and beans were some of the earliest crop L. angustifolius
plants to be cultivated. In lupins it has been possible to observe the String Beans Phaseolus
coccineus
process of domestication because it has taken place recently. Lupinus Carobs Ceratonia siliqua
albus were eaten by the Romans, but were mainly used as fodder.
326 THE FRUITS OF THE EARTH
7.2.5 Vegetables
Tomatoes come sixteenth in the top 30 world crops. Although treated
as a vegetable they are, of course, a fruit. In some dictionary defi-
nitions a vegetable is a plant eaten with an entrée or main course
or in a salad but not as a dessert or table fruit. In fact, in 1893 the
United States Supreme Court ruled that a tomato was legally a veg-
etable rather than a fruit. By this definition a vegetable may originate
from any part of the plant, including the flower (e.g. globe artichoke).
Tomato was widely cultivated in the Americas before the arrival of
Columbus. Aubergines (eggplant), chillies and green peppers are also
fruit-vegetables from the potato family Solanaceae.
7.2 PLANTS FOR FOOD 329
There are about 35 species of Musa (banana). The wild ancestors are
the species Musa acuminata and M. balbisiana. Wild plants have a pulp
that does not develop unless seeds are present but mutant varieties
have a pulp that starts to develop even when the flower is not polli-
nated. Further mutation of these parthenocarpic clones gave rise to
seed-sterile parthenocarpic clones. This may have occurred indepen-
dently in M. maclayi to give rise to the Fe’i bananas of New Guinea.
Hybridisation occurred between M. acuminata clones and between
M. acuminata and M. balbisiana. This latter cross enabled bananas to be
cultivated outside the moist tropics of their origin in South East Asia
and in areas of seasonal drought. The hybrids are triploid or tetraploid
and are more vigorous. Cultivation spread thoughout the Old World
tropics by the end of the sixteenth century when they were then
introduced to Central America. Cultivation of the banana became an
expression of imperialism as U.S. fruit companies came to dominate
the trade. Relatively few clones are grown, exposing bananas to a sig-
nificant risk of disease from banana wilt (Panama disease), or leaf
Figure 7.8. Banana
spot, the pathogenic fungi adapted to attack individual banana geno-
(Musa acuminata).
types that are grown on a large scale.
7.2 PLANTS FOR FOOD 331
7.3.1 Timber
The timber from trees has enabled the construction of extraordi-
nary buildings like the cathedrals of Europe, but there is no better
example of the value of timber in construction than the tremendous
wooden ships that have been built in past ages. In the British Navy,
oak (Quercus) was the favoured species but pine was also important.
The craft that permitted first colonisation and then trade across the
vast distances of Polynesia were constructed of many timbers but at
their heart were vesi logs (Intsia bijuga) from Fiji, hollowed because
of their great density. The maintenance of timber supplies for the
British Navy moulded aspects of foreign policy throughout the eigh-
teenth and early nineteenth centuries; keeping the Baltic open for
trade in the Napoleonic era, gaining Minorca in the Mediterranean
and so forth.
Some species have been particularly favoured because of their rot-
resistant qualities. Teak (Tectona grandis) was used for the keel of HMS
Victory, although elm (Ulmus) was more commonly used for this pur-
pose. Teak is native to India and Malaysia. Natural forests have been
extensively exploited and plantations have been established in the
Philippines and Indonesia. It has been highly favoured because of
its durability, resistance to insect attack and the weather. Satinay
7.3 PLANTS FOR CRAFT AND FUEL 333
7.3.2 Fibres
Fibres from plants have been woven into fabrics for millennia. A large
proportion of harvested trees are not utilised for timber but as a
source of fibre as wood pulp for paper or the production of boards.
It is the cellulose that is most wanted; the lignin that is present
can cause discoloration and make a fibre more brittle, though it is
resistant to decay. Flax and ramie (Figure 7.12) are mainly cellulose
and are white. They provide a fine fibre. Jute and hemp are coarse
and brownish, and contain 10%--15% lignin.
Of much less significance today are the fibres from barks, often
beaten into sheet-like cloths directly. The most famous is the tapa
cloth of Polynesia and New Guinea obtained by soaking and pounding
with mallets the bark of the paper mulberry (Broussonetia papyrifera).
Cork used in bottling wine comes from the cork oak Quercus suber,
which is widely cultivated in the Mediterranean region.
Papyrus was an early form of paper made from the sedge Cyperus
papyrus. Rice paper of the Orient was made by pounding sheets spi-
rally cut from the pith of the rice paper plant, Tetrapanax papyrifera
(Araliaceae). The Aztecs and Mayans used the bark of a Ficus species
to make a kind of paper not unlike papyrus.
Paper making was first perfected by the Chinese about 2000 years
ago. Using the stem fibres of paper mulberry separated in water and
floated, they were allowed to settle on a mesh, before drying. Most
paper today is made from the fibres of woody plants. The first step
is to turn the wood into a pulpy mass. Several methods are used.
In one process wood chips are cooked with bisulphites and then
digested with strong acids. The softened fibres are then blown to
separate them. Paper produced by this process has a tendency to dis-
colour and become brittle with age. The alternative process is alkaline
sulphate production using sodium sulphate, sodium sulphide and
sodium hydroxide, a process that also removes resins from conifer
wood. Acid-free paper is normally used for books.
Purified wood cellulose is used in the manufacture of cello-
phane or rayon depending on the way in which it is extruded in
manufacture.
Rubber
Rubber, Hevea brasiliensis, was exploited exclusively from the wild
forests of South America until it was introduced to South East Asia.
The first plantation was established in Sri Lankla in 1872. A few plants
sent to Singapore, Malaysia and Indonesia were used to establish com-
mercial plantations there. Several other species have been used to
provide latex for rubber but none has really become commercially
viable except when rubber has been in short supply. Gutta percha
(Palaquium gutta) provides a rubber that is more brittle. Manilkara
bidentata provides balata rubber, which is also non-elastic and used to
make machine belting. It is also sometimes used as a substitute for
chicle, a terpene gum from the latex of the sapodilla tree (Manilkara
zapota), the chewing gum of the Aztecs.
Dyes
When westerners travelled to the Pacific Islands they were impressed Figure 7.15. Castor oil from
by the tattooing they observed, produced from a blue pigment pre- Ricinis communis is used in the
pared from the baked nuts of the candlenut tree Aleurites moluccana. production of nylon and other
The fashion was adopted by sailors and exported to the west. Indigo, synthetic resins and fibres. It is
a deep-blue and fast dye, from woad (Isatis tinctoria) was used to paint first converted to sebacic acid.
the body in Ancient Britain. Described by Caesar when he invaded
Britain, it may even have given Britain its name from the Celtic word
‘Brith’ meaning paint or mottled. Indigo was also used as a dye of
fibres, even used to dye the first blue uniforms of British policemen.
Indigo is also obtained from various legumes (Indigofera tinctoria, I.
suffruticosa).
Henna (Lawsonia inermis) is the orange-red counterpart of woad but
is still used to dye the body and hair, especially in the region from
North Africa to South Asia. Its main dye component is lawsone, a
quinine. It is a very fast dye and can also be utilised to dye fabrics
and leather. Juglone obtained from a diversity of walnuts (Juglans), is
also a quinine. Confederate grey is obtained from butternuts (Juglans
cinerea). Bloodroot (Sanguinaria canadensis) provides another red dye.
Many plant dyes have been supplanted by chemically produced
aniline dyes. Such is the case with the red dye (alizarin) produced by
various species of madder (Rubia cordifolia, R. peregrina, R. tinctorum).
However concern for the use of natural products as food additives
has maintained the use of foodstuff dyes. Bixa orellana (Figure 7.17) is
the source of annatto (mainly a carotenoid called bixin) the yellow
dye utilised in many food products such as margarine. Crocetin is
Figure 7.16. Rubber tree
a related carotenoid; the main dye in the stigmas of saffron (Crocus
(Hevea brasiliensis) cut to release
sativus) is used as a spice as well as a dye. It has an ancient use and
the latex in a plantation in Malaysia.
importance, hence the saffron-coloured robes of members of several
religious orders. The spice turmeric (Curcuma longa) has increasing use
as a yellow food colourant.
7.3.4 Fuel
Throughout human history wood has provided the primary source
of fuel. It is only in the past few hundred years that fossil fuels have
338 THE FRUITS OF THE EARTH
Table 7.9 Culinary herbs from the three most important families as sources
Constantinople (See Figure 7.18). In the Middle Ages Venice and Genoa
controlled the trade with the rest of Europe.
There was pepper (Piper nigrum: Piperaceae) from southwestern
India, cardamon (Elettaria cardomomum: Zingiberaceae) from India to
western South East Asia, cinnamon (Cinnamomum zeylanicum: Lau-
raceae) from Sri Lanka, Cassia bark or Chinese cinnamon (C. aro-
maticum from further east), and ginger and turmeric (Zingiber officinale
and Curcuma longa both Zingiberaceae) from Malaysia. From the fur-
thest east and the most valuable of all were cloves (Eugenia caryophyllus:
Myrtaceae) from the South Moluccas and centred on Amboyna, and
nutmeg and mace (Myristica fragrans: Myristicacae) from the Banda
Figure 7.18. Part of the spice
Islands just west of New Guinea. Nutmeg is the seed, mace is the aril
market in Istanbul.
that surrounds it. It originates from the 40 square miles of the Banda
Islands far to the east of the East Indies. Nutmeg was used as flavour-
ing, for example in ale, but also gained a high value as a prophylactic
against plague.
One aspect of the westernisation of the world was the attempt to
gain and control the trade in cloves and nutmeg. In the Middle Ages,
with the spread of the Ottoman Empire, the age-old route of supply
from the Spice Islands via Arabia to Egypt and thence to Venice was
disrupted. Now the maritime western European nations, first Portugal
and Spain, then Holland and England, sought supplies directly from
the Indies and so began their conquest of the world. The competi-
tion between Portugal, Holland and England for a part of the trade
was intense and often brutal. The Dutch East Indies company V.O.C.
(Vereenigde Oost-Indische Compagnie) and the East India Company
(John Company) vied for command. After the Amboyna massacre in
1629 the Dutch gained unchallenged mastery from Portugal and Eng-
land in the East Indies and a monopoly of trade there that was to last
Figure 7.19. Cinnamon for a century. It was finally destroyed when, in 1770, a French botanist
(Cinnamomum zeylanicum). called Pierre Poivre smuggled nutmeg and clove seeds out. In 1796
under the pretext of the Napoleonic wars the English invaded Banda
and transported nutmeg plants to British colonies. Soon an alterna-
tive industry was established in the West Indies, especially Grenada.
Subsidiary trades were established in Asia, initially to finance the
spice trade, that in time became more important than the spice trade
itself: cloves for salt in the Persian Gulf, cloves for gold or opium in
India, opium for gold, silver, silk and tea in China. Cotton fabrics and
china porcelain were carried as well.
Flavourings from the Americas include chilli peppers (Capsicum),
vanilla from the orchid Vanilla planifolia (Figure 7.21) and cocoa from
Theobroma cacoa.
It is a remarkable fact that these three flavourings were combined
with honey in the drink ‘Chocolatl’ that was consumed in large quan-
tities by the Aztecs, in a custom they probably learnt from the south.
They believed that the cocoa tree was of divine origin. They obtained
Figure 7.20. Myristica fragrans,
cocoa from Central America by trade. Indeed cocoa beans were even
source of nutmeg and mace.
a form of currency. Cortés brought cocoa beans back to Spain in
7.4 PLANTS FOR THE SOUL 341
had a long history. Pliny had reported the use of the ashes of a rose
gall, looking like a ball of down, to be mixed with honey and applied
to a bald head, to make hair grow. Man’s vanity and credulity has not
changed much in two thousand years. Some remedies, by happy acci-
dent, were effective (Figure 7.24). The root of mandrake, Mandragora
officinalis, shaped like a man, was especially powerful. It was used to
put people to sleep before surgery, and used along with henbane and
opium, but if its strength was miscalculated the anaesthesia became
permanent! Similarly the efficacy of Ginseng root, Panax ginseng was
advertised in part because of the similarity of the root to the human
body. It is perhaps the most famous of all Chinese medicines, but
paradoxically its efficacy against anything much has been doubted.
The root contains a wide range of constituents, 2%--3% of which are
‘ginsenosides’, triterpenes and saponins.
Plants provide one quarter of all prescribed medicines. An A--Z of a
few are listed in Table 7.10. Many others have been recommended for
one kind of ailment or another. Not all perhaps, are very efficacious.
However, some plants do provide drugs that have a profound effect
on human physiology. These are the poisons. In different parts of the
world different plants have provided arrow or fish poisons. Most are
sources of alkaloids. A different species of Stephania (S. hernadifolia) is
used as a fish poison in Australia. Aconitine from the monk’s hood
Aconitum (Ranunculaceae) was used in various parts of the Northern
Hemisphere as an arrow poison. Strophanthus and Strychnos in Africa
and Asia, and the latter also in South America, were other sources.
Chondrodendron and Curarea (both Menispermaceae) and Hura (Euphor-
Figure 7.25. Catharanthus roseus biaceae) provided other poisons of remarkable efficacy. Hura provides
(Apocyanaceae), a source of
a poison half a million times more toxic than potassium cyanide.
vincristine, a drug that counters
Poisons have also been used to kill people. Socrates, convicted
childhood leukaemia.
of not recognising the gods of the state, introducing new divine
7.4 PLANTS FOR THE SOUL 345
Table 7.10 An A--Z of notable medicines derived from plants to illustrate the range of medicinal plants. There
are hundreds of others
classical world and the native North Americans had obtained their
own acetylsalicylic acid from willow bark (Salix).
One overriding danger for the explorer in the tropics was catch-
ing malaria. There are various legends and stories associated with
the discovery that the bark of a tree native to South America pro-
vided a remedy. In 1633 a Jesuit priest called Father Calancha in Peru
had noted its efficacy. In 1638 the wife of the Count of Cinchon, the
Viceroy of Peru, lay very ill with malaria. The desperate physician suc-
cessfully tried ‘Peruvian bark’ and a remedy was borne. Peruvian bark
was exported by the Jesuits to Rome, at that time a highly malarial
location. Its use spread throughout Europe.
In the eighteenth century Joseph de Jussieu described the tree. Lin-
naeus later named it Cinchona after its first famous recipient. In 1820
the French chemists Pelletier and Caventou isolated the active com-
ponent of the bark, the alkaloid quinine. The value of the bark was
so great that the Dutch and the British attempted to break the South
American monopoly. Joseph Banks was the first to suggest the collec-
tion of the species of cinchona from the Andes. Clement Markham,
who had retired at the age of twenty-one from the Royal Navy to
become an explorer, managed to persuade the Indian Office and
Hooker to fund an expedition to collect Cinchona trees and transport
Figure 7.27. Quinine. them to India for cultivation, some via Kew, some directly to Calcutta.
The transfer, made between 1852 and 1854, was made possible only
by the invention of the Wardian Case, a kind of transportable mini-
glass-house. Meanwhile, in 1852, Hasskarl the Dutch director of the
botanical garden in Java entered South America under a false name
and bribed an official with a bag of gold for some Cinchona seeds.
The results of these competing efforts were a relative failure. The
plants gained were low-yielding varieties. An alternative source was
from an Australian called Ledger who persuaded an Aymara Indian
called Incra to smuggle seeds of high yielding plants out of Bolivia.
Incra was successful but was later discovered and tortured to death.
Ledger failed to sell his seed to Britain. They were wary because plants
previously supplied by Ledger were low yielding. The Dutch govern-
ment took the chance and thereby a multi-million dollar industry was
established in Java based on high-yielding C. ledgeriana. At one time
it produced 97% of the world’s quinine, which was traded through
Amsterdam. The South American industry based on wild trees was
destroyed. However, the capture of Java by the Japanese, and Amster-
Figure 7.28. Neem (Azadirachta
indica). Chewed neem twigs keep
dam by the Germans in the Second World War, gravely threatened the
teeth healthy and neem extract, allies ability to fight in the tropics. This re-ignited the South Ameri-
containing salannin, is now can industry and also the search for synthetic substitutes that, after
included in some toothpastes. the war, eclipsed the use of quinine.
Neem oil repels insects of many Although several effective drugs, like aspirin and quinine that
sorts including mosquitos, chiggers started out as natural plant products, have now been replaced by
and ticks, lice and scabies and is a synthetic product or a synthetic analogue, plants are still a store
also fungicidal, bactericidal and
of huge potential. There is no better example than the Neem tree
antiviral. It has also been used as a
(Azadirachta indica). It has been used for hundreds of years in India
contraceptive douche.
and Burma and is a veritable cure-all.
7.4 PLANTS FOR THE SOUL 347
7.4.3 Beverages
Plants have also provided recreation. Teas of various sorts made from
infusing leaves or roots with boiling water, have been used for millen-
nia. As well as extracting the chemicals from the leaves, boiling water
had the benefit of sterilisation when water sources were likely to be
polluted. Mint (Mentha) tea is popular in Islamic cultures. The mints
contain the essential oil menthol, menthone and menthyl acetate,
flavoured with many other minor components good for indigestion
and colic. Valerian tea (Valeriana officinalis) is noted for its sedative
effects, probably induced by the iridoid alkaloids called valepotriates.
Pacific Islanders prepare Kava from the rhizomes of Piper methysticum.
A mixture of different lactones produces a feeling of brotherhood and
tranquility when administered in the formality of the Kava ceremony.
Like the ritualistic drinking of wine, a few drops are allowed to fall
to the floor as a libation to the ancient gods. The three most impor-
tant components are kavain, dihydrokavain and dihydromethysticin.
The first anaesthetises the mouth like cocaine but the second is more
readily absorbed and metabolised.
The most widely used teas are stimulants and most, including ‘tea’
itself, contain caffeine. The caffeine content of the raw product does
not really indicate the caffeine ‘hit’ that a beverage provides because
of the different ways they are prepared and the strength of the brew.
Typically, a cup of instant coffee can have more than twice as much
caffeine as a cup of tea brewed for 1 minute. Ground coffee has much
more but so has stewed tea. Cocoa has a quarter the caffeine of tea, but
chocolate has more. Theobromine is a weaker stimulant than caffeine, Figure 7.29. Caffeine.
and is also found in tea and maté. Colas of various sorts rival instant
coffee for their caffeine content. In recent years guarana (Paullinia
cupana), used with cassava to make an alcoholic beverage in the Matto
Grosso, has been widely added to alcopops to make stimulant or reviv-
ing drinks because of its high caffeine and theobromine content.
The Chinese emperor Shen Nung discovered green tea in 2737
bce, from Camellia sinensis, when some leaves fell into his drinking
bowl. The Portuguese probably introduced tea to Europe from the
Far East. By the early nineteenth century a huge trade through the
port of Canton, probably half to Britain, was in place. It was the tax
on tea re-exported to America that was used as one excuse for the
rebellion that led to the War of Independence of the United States:
‘no taxation without representation’. Chinese civilisation was brought
low by other westerners by the sale of opium, traded for tea, among
other items. Introduction of tea plants from China to India had failed,
but then Wallich, once director of the botanic gardens in Calcutta,
identified a native Indian variety of tea plant in the hills of Assam
that became the foundation of the Indian tea industry. Today tea
plantations are found throughout the highlands of Asia and Africa
(Figure 7.31). For a long time Indian and Sri Lankan tea was regarded
Figure 7.30. Cocoa tree
as inferior in quality to Chinese tea. Green Chinese tea has the tannin
(Theobroma cacoa) with
epigallocatechin as its main flavour component. The tannins in black
cauliflorous fruits.
fermented tea are oxidised and very complex.
348 THE FRUITS OF THE EARTH
Like many plants used for pleasure, the drinking of tea became the
centre of a ritual in both Britain and Japan. Different varieties, condi-
tions of growth, and treatment after harvest, result in the subtle dif-
ferences in taste and colour: Assam, deep bronze and malty; Ceylon,
pale gold and delicate; Darjeeling, light and fragrant; Kenyan, cop-
pery and strong; Lapsang Souchong, smoky. It is curious that some of
the more specialist teas like Earl Grey, with its citrus and bergamot,
arose firstly as teas adulterated with other plant material to make up
bulk and weight before they were traded.
Coffee is another Old World species. It probably originated as a
crop in Ethiopia. Its oldest recorded use is as the leaves or beans
chewed to relieve fatigue and hunger. Coffee drinking originated in
Arabia in the fifteenth or sixteenth century and spread via Turkey
to the rest of the world. Coffee cultivation was introduced to the
east from plantations in Yemen, especially by the Dutch who estab-
lished plantations on Java by the late seventeenth century. There were
two main original introductions to the New World. One was via the
Amsterdam botanical garden of a single plant sent from Java. This was
the source of a few seedlings sent to the Paris Jardin des Plantes that
were then sent to Martinique. Another introduction was from Yemen
via Réunion and then to the Caribbean. As a result the genetic base
of New World coffee is very narrow and it is very vulnerable to leaf
rust (Hemileia vastratix).
Maté (Brazilian or Paraguay tea) or Ilex paraguarensis, provides a
caffeine-rich tea that is popular in South America. Wild trees are
also harvested, along with a few related species to supplement the
plantation supply.
Kola tree (Cola nitida and C. acuminata) originated in West Africa.
The nuts that provide the caffeine rich flavouring of many soft drinks
7.4 PLANTS FOR THE SOUL 349
are actually the embryos after the fleshy seed coat is removed. Kola
is a relatively recent domesticate, within the past 1000 years or so.
Sumerians made bread with wheat and barley and then fermented
bread crumbs to create an alcoholic beverage called Sikaru sucked
through reeds as straws to avoid the debris.
Alcohol has also a long history of medicinal use. The strong beer
produced in classical times called Zythum was a component of many
medicinal remedies. Medicines were dissolved in it, and in previous
centuries it was given in great quantities to the ill. At least, if drunk
in large enough quantity, it kept the patient quiet. It was not until the
late Victorian era that hospitals were founded in Britain on the basis
of strict abstinence. But it is not so long since stout was marketed
as being ‘good for you’. Although today, advertisers might be wary of
claiming medicinal value for alcoholic beverages, who can doubt the
profound pleasure and soothing of the soul that alcohol can bring
and not just from intoxication?
The most important alcoholic drinks are made from grain or from
grapes. Barley is the grain used most often to make beer and spirits.
It is first soaked and then allowed to germinate so that the starch
is turned into sugar. Germination is brought to a halt by baking.
The temperature and length of time baking helps to determine the
flavour. Bourbon is distilled from a mash of grain containing, accord-
ing to US Federal Law, not less than 51% corn, along with barley
and either wheat or rye. Each distillery has its own unique blend
of grain and some of the mash recipes are generations-old family
formulas jealously guarded. In Africa, sorghum and millet are fer-
mented to make alcoholic porridge and beer. Some notable spirits
Figure 7.33. Barley (Hordeum
have other sources of carbohydrate than grain. Vodka is made from vulgare).
grain or from potatoes. Cassava is harvested in Brazil for industrial
alcohol production. Tequila is usually clear in colour and unaged
and is distilled from the fermented juice of the Mexican Agave
plant, specifically several varieties of Agave tequileana (Figure 7.34).
Mescal, a similar beverage to Tequila, is less expensive and stronger
in flavour, and is made from an agave plant that grows wild in the
Oaxaca region.
As important as the source of carbohydrate for fermentation are
the many plants used to give flavour to alcoholic drinks. Honey and
dates were used to flavour Sumerian Sikaru. The Ancient Egyptians
used juniper, ginger and saffron to flavour their own strong beer
called heget or, in Greek, zythum. Distilled alcohol is a pretty flavour-
less substance. Other plants add flavour, whether it is the oak of
sherry barrels used to age whisky or the wood charcoals used to fil-
ter bourbon. Bombay sapphire gin has ten different ‘botanicals’, the
350 THE FRUITS OF THE EARTH
most important being juniper berries and coriander. Gin gets its name
from the Dutch word genever, meaning juniper. The reputation of gin
to bring on a miscarriage may be related to the effects of juniper. Beer
gains its bitterness and aroma from hops Humulus lupulus which also
prolongs the life of beer. Hopped beers were established in Medieval
Europe and when they spread from Holland to England in the Tudor
period the native brewers of unhopped ale complained and tried to
prevent it.
Absinthe has a fascinating history. In little more than a century,
between the writing of the original recipe by Dr Pierre Ordinaire in
1792, and the founding by Henri-Louis Pernod of the most impor-
tant absinthe distillery in France in the early 1800s, to its banning
in France in 1915, it came to be favoured in the bohemian circles
of France for its ability to stimulate creative activity. Its users and
abusers included the poet Rimbaud, the writer Baudelaire and the
painter Van Gogh, among many others. Absinthe is an emerald green
alcohol, as a result of the presence of chlorophyll, with added herbs
(aniseed, fennel, hyssop, lemonbalm, angelica, star anise, dittany,
juniper, nutmeg and veronica), the most important being the bit-
ter wormwood (Artemisia absinthium). The name wormwood denotes
its former use to counteract parasitic worms. Vermouth, made from
the flower heads of wormwood, gets its name from the German for
wormwood (wermuth). Up to 90% of wormwood oil is thujone, also iso-
lated from Thuja occidentalis and other plants. The psychoactive role
of thujone is uncertain, but the related species Artemisia nilagirica
was smoked in West Bengal for its psychoactive effects, and Artemisia
caruthii was inhaled by the Zuni native Americans as an analgesic.
Calamus (Acorus calamus) and nutmeg (Myristica fragrans) were also
Figure 7.35. Hop (Humulus sometimes used in making absinthe and may have enhanced the psy-
lupulus) is a climber related to choactive effect. Absinthe was diluted with cold water poured over
Cannabis sativa. It is dioecious; the a perforated spoonful of sugar, turning the shot of absinthe milky
female flowers have bitter
white as the essential oils were precipitated out of the alcohol. Much
alkaloids.
of the effect of absinthe was purely alcoholic. Undiluted absinthe
7.4 PLANTS FOR THE SOUL 351
had 60%--85% alcohol so a large part of its peril was associated with
alcohol abuse.
Wormwood is used to flavour the Swedish brannvin made from
potatoes. Chartreuse, made by Carthusian monks supposedly follow-
ing an ancient recipe called the ‘Elixir of Life’, contains 130 herbs
and spices, including small amounts of thujone. So also does Bene-
dictine, which is made by Benedictine monks. Other drinks no longer
use wormwood. Herb Sainte, from New Orleans, and Pernod are
wormwood-free absinthes but contain star-anise (Illicium verum) for
flavour. Pastis is a similar liqueur to absinthe and was also originally
made with wormwood, but is now flavoured with liquorice (Glycyrrhiza
glabra). Other essential oils are used to flavour many other drinks like
Ouzo and Jägermeister.
Wine is one alcoholic drink that requires no adulteration but it
too provides an example of the ambivalence there is about the use of
plant products for pleasure. Dionysus, the god of wine, was the son of
Zeus and a mortal woman. He taught the art of vine cultivation and
gave the gift of wine, but he has two natures, bringing joy, health
and divine ecstasy, or brutality and unthinking rage. He was accom-
panied by the Maenads, drunken women bearing rods tipped by pine
cones (a reference, perhaps, to the use of resin to preserve wine), and
who might go mad and rip apart and eat animals raw. Dionysus was
associated with rebirth after death, like the vine growing back after
it is pruned. Wine conferred a feeling of power as if by drinking it
the drinker gained part of the divinity of Dionysus himself. There are
echoes here in the use of wine in the Eucharist as a celebration of
the Christian faith.
Wine was also associated with creativity. Most of the Greek plays
were first performed at the feast of Dionysus. Nietzsche contrasted the
creativism of Apollo with that of Dionysus: the first cool, structured,
full of meaning and controlled; the second unpredictable, instinctual,
wild, ecstatic, pleasurable and emerging from uncontrolled Nature.
The Dionysian cult magnified the access to the natural world by use
of fennel Foeniculum vulgare (Apiaceae).
The range of grape varieties allows wines to be savoured of such
subtle difference and speciality (Table 7.11). Grapes (Vitis vinifera and
other species) are widespread throughout the Northern Hemisphere.
The grape vine was probably domesticated in South West Asia, spread-
ing from there to reach Greece about 3000 years ago. When the Asian
grape was introduced to North America it hybridised to native grape
species especially V. labrusca. American grapes are resistant to the
root louse Phylloxera and after an epidemic in 1867 they were widely
introduced to Europe for use as rootstocks. The dried fruit, raisins,
sultanas (seedless) and currants (from Corinth), are particularly
rich in anti-oxidant compounds, especially the phenolic compound
resveratrol.
Alcohol has fuelled the work of many artists and writers and
destroyed the lives of not a few. Unfortunately the excessive use of
alcohol does not guarantee the production of great artistic work.
352 THE FRUITS OF THE EARTH
Cabernet Sauvignon Deep red Complex, depth of fruit flavours, blackcurrant, blackberry,
long maturing
Merlot Red More acid than above and faster maturing
Shiraz, Syrah Red Luscious, silky, spicy
Grenache (Garnacha) Red or Rosé Sweet, fruity, low tannin
Pinot Noir Red Delicate fruits and flowers to rotting vegetables, perhaps the
oldest variety
Gamay Red Beaujolais, acid but low in tannin
Chardonnay White Light and subtle but often heavily oaked
Sémillon White Dry or sweet, yellow, with hints of citrus
Sauvignon Blanc White Light with a touch of dryness, enjoyed young or slightly aged,
made more robust by fermenting in oak
Riesling White German, sweet and fragrant with a touch of spice
Muscadet White Extremely dry, and light
Muscat Red or White Provides fruit as well as wine
(a) Not all plant products used for pleasure have a psychoactive com-
ponent. Chicle collected from the latex of Manilkara zapota trees in
Central America provides the base for chewing gum. It contains no
active components itself, though mint and other flavourings are nor-
mally added, but the process of chewing encourages the release of
natural endorphins.
(b)
7.4.6 Scents and perfumes
The word ‘perfume’ comes from the Latin per fumen (through smoke),
a reference to the use of incense in religious ceremonies. The same
scented flowers cultivated by the Ptolomaic Egyptians are favoured in
gardens today: jasmine, rose, lily-of-the-valley and stock. Flowers were
grown in gardens in the Roman Empire for garlands and for perfume,
(c) and there was an extensive luxury trade in flowers. Egypt exported
fresh flowers to Rome! The technique of distillation was established
by Islamic chemists. Centres such as Damascus were famous for the
perfumes they produced. The distilled scent of Damask rose produced
a lasting perfume that was mainly the result of two components,
geraniol and 2-phenylethanol.
Distillation involves the passing of steam through the flowers so
that it becomes laden with volatile oils, and then allowing it to con-
(d)
dense. The insoluble oil is then drawn off. Around 2000 roses yield
just 1 g of the attar of roses. Alcoholic extracts of perfumes were first
produced in Europe in the Middle Ages after contact with Islamic sci-
ence. Various parts of the plant were used. The process today involves
either cold-pressed extraction, extraction with ether, or steam distilla-
tion, and then washing and dilution with alcohol. Roses, violets, jas-
(e)
mine, tuberose, mimosa, jonquil, orange-blossom and bergamot from
the Mediterranean region, plus lavender and peppermint from more
northern regions are the most important sources of scented essen-
tial oils. Alcoholic extracts are complex mixtures. Bergamot from
Citrus bergamia contains α-pinene, β-pinene, myrcene, limonene, α-
bergaptene, β-bisabolene, linalool, linalyl acetate, nerol, nery acetate,
geraniol, gerianiol actetate and α-terpineol.
(f)
7.5 The scientific improvement of plants
Flowers hold a central place in human history. The use of the word
‘flower’ for ‘the best’, ‘the most attractive part’, ‘the essence’, and the
way the word ‘flowering’ is used to describe a new cultural develop-
ment, are a measure of the central place of flowers in our culture.
Agriculture had separate origins in Western Asia, Central America and
China. The earliest traces provide abundant evidence for the botani-
cal knowledge that gave rise to civilisation. Even the monuments are
marked with patterns derived from plants.
cornflowers from Egypt, and the Sumerian caps, crowned with gold
daisies, that can be seen in the British Museum.
Plants have had an important symbolic significance. Olive foliage
was the sign of goodwill (the olive branch). Cherry laurel (Prunus
laurocerasus) was used to crown the Caesars, perhaps quite appro-
priate considering their later murderous behaviour, since the leaves
contain cyanide that is released when they are damaged. The rose,
sweet scented and full of soft petals, was associated with luxury, with
Venus, with love and spring, but also with death. Garlands of roses
were placed as wreaths at tombs. This was justified in early Chris-
tian times because, with its thorns, it also came to symbolise Christ’s
agony. Flowers as garlands or chaplets were incorporated into many
religious ceremonies. The cult of the Virgin Mary resulted in many
flowers being baptised with Christian names. Calendula (Marigold),
Alchemilla (Our Lady’s mantle), Spiranthes (Our Lady’s tresses), Cardamine
(Our Lady’s smock), Anthyllis (Our Lady’s fingers) are just some of them.
Flowers also entered heraldic imagery. Broom (Genista) was the symbol
of the Plantagenet dynasty (planta-genista).
This kind of floral imagery is very ancient and widespread. Perhaps
the Indus Valley civilisation of 5000 years ago provided the precur-
sor for the strong identification with nature and the sacredness of
plants in Hinduism. The lotus blossom had a paramount significance
but many other plants like the bright yellow and orange flower gar-
lands of marigolds were favoured in ceremonials and also in private
life. Garlands were a bed-time adornment of men as well as women.
Jasmine flowers were used to dress the hair.
‘Say it with flowers’ was a slogan coined for the American Society
of Florists, but the Language of Flowers was quite literally an attempt
to systematise the symbolic character of flowers. In a book published
in Paris in 1819, Charlotte de Latour codified the language of flowers
Figure 7.43. The derivation of
by providing a dictionary of meanings. It is all very amorous and
the fleur de lis symbol. Some
ridiculously detailed. A rosebud with its thorns and leaves signified
writers identify the Fleur de Lis
(flower of Louis) as a lily but it is ‘I fear, but I am in hope’, while without its thorns it meant ‘there is
probably an Iris florentina (top), the everything to hope for’. Without its leaves meant ‘there is everything
source of the violet-scented to fear’, and when upright but upside down meant ‘One mustn’t fear
insecticidal and medicinal orris or hope’. A marigold on the head meant trouble to the mind, on
root. the heart, the pain of love, and on the breast, boredom. The whole
nonsense, which became extremely popular, and was elaborated by
many other authors, was given the gloss of being an ancient science
practised in classical times and the Orient.
There is rosemary, that’s for
A different symbolic meaning has been given to the same flow-
remembrance . . . and there is
pansies, that’s for thoughts . . .
ers over the ages. In Shakespeare’s Hamlet the deranged Ophelia gives
Shakespeare fennel to the King signifying flattery and columbines to the Queen sig-
nifying adultery. The symbolism is poetic and complex. Three flowers
are supreme in their symbolic weight: the lotus, the rose and the lily.
The lotus (Nymphaea coerulea) is the blue lotus (actually, a water-lily)
that was sacred in Ancient Egypt. Its flowers open at dawn and close
at night and so it became associated with Ra the Sun god. The bud
clearly had a phallic significance too. The flowers are fragrant. There is
7.6 THE FLOWERING OF CIVILISATION 363
also a white water-lily, the true or sacred, N. lotus that opens at night
and also grows in the Nile delta. The Indian Lotus (Nelumbo nucifera),
was introduced in the Persian period. The Madonna lily (Lilium can-
didum) figured on Cretan frescos from 5000 years ago. It is native to
the eastern Mediterranean region but has long been cultivated for
its white flowers, used for making scent. White lilies are mentioned
in the Bible, but some have suggested that the Rose of Sharon may
be L. candidum. Another suggestion is that this is Pancratium mariti-
mum (or Sea Daffodil), while the Lily of the Field is Narcissus tazetta or
Hyacinthus orientalis. The sweet-smelling lily was identified with spring-
time and rebirth in the Roman period. In the early Christian period
it was rejected for being a symbol of luxury and idolatry but later it
came to symbolise purity and was associated with chastity and the
Virgin Mary.
There was also a cult of flowers and gardening in China, even
a peony mania in the early ninth century. Peach, chrysanthemum,
lotus, peony, Cymbidium (orchid) and Lilium lancifolium (tiger-lily) were
all cultivated for their beauty from 1000 bce. From about 600 ad The deep green foliage is quiet and
many others like camellia and magnolia were also cultivated. Gar- reposeful.
The petals are clad in various
dens provided a quiet retreat from the world where the beauty of
shades of red.
nature could be contemplated. The arts of poetry and painting were
The pistil drops with melancholy.
intimately connected with the study of flowers. (See, for example, Wondering if spring knows her
the poem describing the peony, on this page.) The four noble plants intimate thoughts.
were the plum, bamboo, orchid and Chrysanthemum. Chrysanthemum, Chinese poem about the
the flower of autumn, was the symbol of joviality and contentment. peony
Bamboo, for spring, was the symbol of the courteous gentleman, and
of companionship and modesty. The orchid, for summer, was the sym-
bol of the refinement of beautiful women and great men. The plum,
symbol of winter, was for chastity and feminine beauty and also had
a complex number symbolism: the blossoms are Yang, Heaven, the
branches, Yin, Earth, the pedicel is the Ridgepole of the Universe,
the three sepals are Heaven, Earth and Man, the petals are the five
elements and the stamens are the seven planets.
new cultivars. Tulips were not popularised until about 1608 in France
but soon a craze started which spread north to Holland. By 1629
Parkinson, in perhaps the first great garden book, the Paradisi in Sole,
numbered 140 different varieties in English gardens. Huge sums were
risked on the newest varieties. One bulb cost a carriage and pair;
another cost twelve acres of land. In Haarlem one merchant bullied a
rival into selling a duplicate bulb for 1500 guilders and then stamped
on it to preserve the value of his one. A seaman accidentally mistook
another bulb worth 3000 guilders for an onion and ate it. He ended
up in jail for six months. Soon ‘paper’ tulips, futures on potential
tulips, were being traded, but in 1637 the bubble burst, ruining many
speculators. However, the enthusiasm for flowers did not disappear.
The opening up of the New World provided an immense source
of new plants -- many of which could grow very well in the gardens
of north-west Europe. Aristocratic collectors competed by financing
collectors to improve their stock. John Tradescant laid out a garden
for Robert Cecil, Earl of Salisbury, at Hatfield House and later served
the first Duke of Buckingham and Charles I. His own garden in Lam-
beth became a treasury of exotic plants from abroad. His son John
Tradescant the Younger continued the tradition; he travelled to the
north coast of Africa, and made three trips to Virginia. Many North
American flowers were introduced to Europe through the Tradescant
garden. They include the tulip tree, cornflowers, Michaelmas Daisies,
Virginia Creeper and, of course, Tradescantia. In France another father
and son team, Jean and Vespasian Robin, were as influential. Their
Paris garden was later to transmogrify, much enlarged, into the Jardin
des Plantes. The black locust introduced from North America, but
probably first grown in the Tradescants’ garden, was given the name
Robinia pseudoacacia in their honour. The close connection with North
America continued throughout the seventeenth and eighteenth cen-
turies. Philip Miller, at Chelsea Physic Garden in London, was eager
to receive seeds from the Quaker farmer John Bartram. Botany was
no insipid past-time but a vigorous and exciting adventure at home
and abroad. Rumbustious botanical excursions to the Physic Garden
caused a public scandal.
It is only possible to mention here a few of the most significant and
intrepid plant collectors. Francis Masson introduced many heathers,
pelargoniums and other plants from South Africa, but after surviving
capture by French privateers and hostile natives, Boers and escaped
convicts, he too died young, frozen to death in North America at the
age of 33.
The story of Philibert Commerson, on the rival French expedition
to Cook’s by Bougainville, appeals because it includes more of the
kind of lunacy and obsession that accompanies many of the adven-
tures of these botanical maniacs. Philibert Commerson (1727--1773)
was trained at Montpellier where he got into trouble for stealing
plants for his herbarium from the gardens of residents and even from
the botanical garden. He made his name as a heroic plant collector,
escaping one mountain avalanche by rolling down ahead of it like
7.6 THE FLOWERING OF CIVILISATION 365
7.6.3 Plantscapes
Plants in their natural setting have come to be regarded as ‘her-
itage’ and as an amenity resource. Floras have been transformed and
enriched by the introduction of exotic species. A cult of trees has
never been far from the surface. Trees were associated with national
strength and defence. In the seventeenth century, in his best-selling
book called Silva, a report on tree planting to the Royal Society, Evelyn
noted the loss of yew: ‘Since the use of bows is laid aside amongst
us the propagation of the yew-tree is quite forborn’. He praised oak
because ‘ships of oak become our wooden walls’. Evelyn was a cham-
pion of native trees and the planting of trees not just for their uses
but for their aesthetic beauty.
Towards the end of the seventeenth century and in the eighteenth
century there was a change of sensibility. There was a shift away
from the emphasis on plants for food and for survival to plants for
expression. The landscape artists, either the idealised landscapes of
Lorraine or the romanticism of Friedrich and Constable, and in Japan
the woodcuts of Hiroshige and Hokusai, have all trained our eye. The
clipped geometrically shaped symmetrical gardens of the Restoration,
with their symmetric parterres gave way to rococo asymmetry, which
at its margins blurred the distinction between garden and Nature, and
366 THE FRUITS OF THE EARTH
then there was the exuberance, the wildness, of baroque. Nature and
the countryside were colonised again, but now by the intellect. Just
as towns and cities were starting to burgeon like great excressences,
gardens were now to be constructed to recall an Arcadian landscape
when life was pure and simple. They were to be artfully constructed
to present a picture of an idyllic landscape. The landscaped parks
of William Kent, Charles Bridgeman, Lancelot ‘Capability’ Brown and
Humphrey Repton marked the final phase of taking possession of the
landscape. Now even the wild or semi-natural was to become reformed
in an ideal image as part of the estate of the landowner. Improvement
could be theatrical and painterly as at Stourhead, involving large-scale
works like the diverting of rivers and streams, the damming of lakes
and the moving of mature trees (Figure 7.44).
Gardening on the grand scale can be seen at Blenheim and many
other grand country houses (Figure 7.45). It might also include more
subtle changes of landscape. Views were very important. Through the
views the park seemed to include the countryside around. This could
include, not just scenes of wilderness, with natural features incor-
porated or enhanced, but the productive countryside of fields and
woods. Ha-has, hidden boundary banks and ditches were constructed
so that the riff-raff were excluded, but the eye of his lordship was
unimpeded.
In part, agricultural development funded the development of land-
scaped parks but in its turn the timber of the landscape parks was
an important source of income. Humphry Repton railed against the
nouveau riche who had only a commercial interest, but in time the
improvement came to be seen more pragmatically as necessary invest-
ment for commercial return.
Grand landscape design was in decline by the beginning of Victo-
ria’s reign, but by this time the Romantic Movement had taken psy-
chological possession of the landscape and its flora. The countryside
and Nature became now as much a mental landscape as a real one. At
7.6 THE FLOWERING OF CIVILISATION 367
its most shallow, this was expressed as a search, not just for beauty,
but for the ‘picturesque’, a scene capable of being painted. This was
a way in which beauty could be circumscribed, described, possessed.
It has provided the vocabulary of our appreciation of the countryside
and Nature. Jane Austin poked fun at the cult of the ‘picturesque’ in
her novel Sense and Sensibility published in 1797.
In the works of the Romantic Poets something more sophisticated
and much more important was re-created: an emotional relationship
with Nature. For Wordsworth, ‘Nature’ became a medium through
which the most profound, even religious, thoughts were conveyed.
In his long autobiographical poem The Prelude, Nature could speak
through the medium of a ‘rugged’ landscape, an individual prim-
rose growing from a rock-face, or the wind blowing through some
trees. The romantic poets were writing in the context of the begin-
nings of industrialisation and a world that seemed more and more
mechanistic.
In the same way the long tradition of gardens has led to the devel-
opment of a spiritual space seen to its perfection in the highly arti-
ficial Japanese gardens that still manage to personify Nature (Figure
7.46). It is gardeners and horticulturalists, not botanical scientists,
who now know plants and appreciate their endless forms.
Plants are now manipulated to create artificial habitats that are
pleasing to the eye. Plants are reduced to being tools of the archi-
tect. Street trees soften the line of roads. Parks, squares and gardens
provide a ‘green lung’ to city dwellers. No new office block is com-
Figure 7.46. Japanese garden.
plete without its arrangement of glossy ‘houseplants’ to welcome the
visitor in the lobby. London has six million trees in parks, gardens
and streets. Favoured street trees are those that grow upright and do
not produce slimy honey-dew or leaf litter. It is extraordinary to see
Ginkgo biloba fringing a polluted city street, like the last descendant
of a royal lineage, 200 million years old, reduced to the status of a
street cleaner. But we are thankful for it!
During the nineteenth century the growing appreciation of green
places for the physical health of the populace led to the establishment
368 THE FRUITS OF THE EARTH
of city parks and other preserved spaces. In London, the great nine-
teenth century metropolis, it was the business elders of the City
of London who protected Hampstead Heath and Epping Forest. The
romantic landscape was in some ways a reaction against the narrow-
ing spirituality of the day. In the same way plants have become more
important to us in our dry sterile city lives, reminders of both Nature
and another world. It was John Muir who emphasised the value of
wildness. His efforts led to the preserving of areas of wilderness in
the USA, starting with Yosemite in 1890, leading the way for the rest
of the world.
Walk away quietly in any direction
It has also become so much more urgent for us to protect the alter-
and taste the freedom of the
mountaineer. Camp out among the
native natural plantscape of trees and flowers and rocks and rivers,
grasses and gentians of glacial an other-world that is closer to the infinite and to the mystic. The
meadows, in craggy garden nooks need for a countryside that we can access is strong. Rambling is per-
full of Nature’s darlings. Climb the haps the biggest leisure activity in Britain . . . after gardening. Today
mountains and get their good the spiritual and recreational value of plants rival their importance
tidings, Nature’s peace flow into economically and commercially, but ecotourism is taking an increas-
you as sunshine flows into trees. ing share of the tourism industry. The United Nations designated the
The winds will blow their own
year 2002 as the International Year of Ecotourism (IYE) to promote the
freshness into you and the storms
three basic goals of its Convention on Biological Diversity. It is note-
their energy, while cares will drip
off like autumn leaves. As age worthy though that only one of these is to conserve biological (and
comes on, one source of enjoyment cultural) diversity. The other two were economic and commercial.
after another is closed, but nature’s
sources never fail. 7.6.4 Future plantscapes
John Muir There can be little doubt that plants are going through more rapid
changes now than they have ever done before. It is astonishing to
think how rapidly the landscape has been changed by human beings,
starting with Neolithic culture perhaps a little over 10 000 years ago,
but mainly in the past two centuries. Within a few thousand years
huge areas of the world’s vegetation has become dominated by the
influence of human beings. First, organised pastoralism, and then
7.6 THE FLOWERING OF CIVILISATION 369
from grazing while they establish. In many areas aquatic and riverine
environments are especially vulnerable because of the rapidity with
which exotic weeds can spread along waterways.
Balick, M. J. and Cox, P. A. Plants, People, and Culture. The Science of Ethnobotany
(New York: Scientific American Library, 1997).
Frankel, O. H., Brown, A. H. D. and Burdon, J. J. The Conservation of Plant
Biodiversity (Cambridge: Cambridge University Press, 1995).
Hobhouse, H. Seeds of Change. Five Plants that Changed Mankind (New York:
Harper and Row, 1987).
Lewington, A. Plants for People (New York: Oxford University Press, 1990).
Simmonds, N. W. 1977. Evolution of Crop Plants (London and New York:
Longman, 1997).
Tivy, J. Agricultural Ecology (London: Longman, 1990).
Chapter 8
Knowing plants
things, is therefore the essential reality of the Universe, and the only
material source of natural substances. Heraclitus saw the harmony
of the world as the resolution of many diverse forces. The essence of
Logos creates an infinite and uncorrupted world, without beginning,
and converts this world into various shapes as a harmony of the oppo-
sites, the composition of which sustains everything in Nature. This
concept of unity in diversity, of the ‘One as Many’, is Heraclitus’s
most significant contribution to philosophy. He was one of the first
philosophers to suggest that we cannot rely wholly on our powers of
observation, a suggestion that would have profound implications for
western philosophy for the next 2000 years.
The school of Pythagoras greatly influenced the course of Greek
philosophy, and particularly Plato. Pythagoras, who was born on the
island of Samos, founded an ethical, religious, and mystical system of
teaching about 530 bce in Croton in southern Italy. The Pythagoreans
believed that knowledge was inherently mystical. For them, numbers
were the ultimate elements of the Universe. This may seem a rather
bizarre idea to us but the Pythagoreans thought of numbers spatially.
To say that all things are numbers is another way of saying that every-
thing that exists consists of points in space, which taken together
make a number. There is a link to modern physics here with the use
of string theory to provide a grand unifying theory of everything.
In making number the first substance of the world, the Pythagoreans
transferred these mathematical concepts to material reality. Since the
fundamental realities of the world were structural and mathematical,
those which display greater simplicity, regularity, and coherence in
mathematical proportions or parameters are aesthetically more beau-
tiful and ‘better’. The correct proportion between the whole and its
parts was the cause of beauty in the object, and was called harmony,
meaning perfect arrangement. The similarity between the whole and
its parts can be expressed in terms of some proportion supposed to
exist between them. Pythagorean interests in proportion extended to
music and they devised a musical scale based on vibrating strings of
different lengths with a constant ratio of 3:2. This mathematically ele-
gant system was extended to the Universe since the five planets known
at that time had movements with similar ratios. The Pythagoreans
imagined ‘a music of the spheres’ that was created by the Universe, a
wonderful idea that has inspired many composers in the modern era.
As we saw in Chapter 2, the influences of mathematics, particularly
the Fibonacci Series and the Golden Mean, had powerful impacts on
plant morphology and development in the nineteenth and twentieth
centuries.
The identity of harmony with good order is considered by some
to have been the main contribution to Greek philosophy by the
Pythagoreans. The study of mathematics was indispensible for intel-
lectual and spiritual progress, while medicine was the science that
brought harmony to the body. Ultimately Pythagoreanism has been a
dynamic force in western culture, influencing not only philosophers,
374 KNOWING PLANTS
his writings that became the foundation for later herbals such as
those of Dioscorides and Herophilus of Alexandria. Herbalism was
just one important branch of botanical knowledge that was taught in
the Lyceum of Athens, but it is virtually the only one that survived
until the renaissance of botany in the second millenium, marked by
the reprinting of Theophrastus’s works in the late fifteenth century.
Dioscorides thus represents the final chapter in Greek herbalism. His
Materia Medica, which was written about ad 60 largely replaced the
Rhizotomikon of Crateuas (120--60 bce) and became the basis of Ara-
bic pharmacopeia, and was often accompanied by beautiful illustra-
tions. Theophrastus’s work thus remained influential in the Islamic
world. Nestorian Christians driven from the Eastern Roman Empire
had carried the European classical tradition from Syria to Persia. At
Jundeshapur, a university was established about ad 500 that kept the
tradition alive. Arab herbalists both preserved the classical herbalism
of the west and added to it. For example, Avicenna (ibn Sina) (ad 980--
1037), the foremost Islamic philosopher who came from Iran, pro-
duced the Canon of Medicine, which included many plants unknown
to Dioscorides. The spread of Islam, and the trade and commercial
prosperity that accompanied it, provided cultural links between Per-
sian learning, and that of India and China. In the Islamic centres
of Sicily and Toledo, Jewish scholars translated the classical works
and thus helped to spread botanical knowledge back to the west,
where, after a long period of stagnation lasting almost 1800 years, it
was rediscovered. Meanwhile, in China, botany was developing in a
uniquely independent way.
conditional determination of phenomena, is relevant to the course of A few minutes ago every tree was
plant development and environmental interactions and subsequently excited, bowing to the roaring
on the study of evolution. storm, waving, swirling, tossing their
The genius of Johann Wolfgang von Goethe (1749--1832) claims branches in glorious enthusiasm like
a place here, although in contrast to the idealism of the Nature- worship. But though to the outer ear
philosophers, Goethe’s method was essentially one of empiricism and these trees are now silent, their
songs never cease. Every hidden cell
inductivism. Like Kant, he was well aware that all observations are
is throbbing with music and life,
theory-laden, but his approach was to make the subjective aspect
every fiber thrilling like harp strings,
of observations an integral part of his empirical method since he while incense is ever flowing from
believed that it led to deeper insights. This he did by varying the the balsam bells and leaves. No
conditions under which the phenomena were observed, by studying wonder the hills and groves were
plants throughout their ontogeny. He also paid particular attention God’s first temples, and the more
to malformed plants. His insights were obtained through highly per- they are cut down and hewn into
ceptive observation and intense visual impressions. He was a ‘picture- cathedrals and churches, the farther
thinker’ (equivalent to the ‘intuitive Anschauung’ of Troll), which also off and dimmer seems the Lord
himself.
has been described by Agnes Arber as ‘thinking with the mind’s eye’.
John Muir
He believed in open-mindedness, rejected dogma and took great care
not to replace observations with abstractions. Although he believed
in the harmony of the Universe, he sought revelation of it from the
world of nature through phenomena.
For Goethe, science was not the search for abstract truth, but for
synthetic and dynamic archetypal phenomena (Urphänomen), which,
to him, were the highest levels of experience attainable. His ‘delicate If we are to describe what a body is,
empiricism’, which revealed his distrust of reason, was the approach the whole cycle of its alternations
that led him to formulate the Urphänomen. Unfortunately there has must be studied; for the true
been much confusion over Goethe’s concept of Urphänomen. It would individuality of body does not exist in
be a mistake to attribute a Platonic Idealism to Goethe, for Plato’s a single state but is exhausted and
universals are not derived by empirical means. Goethe’s Urpflanze displayed only in this cycle of states.
Hegel
has been erroneously interpreted as equivalent to an actual ancestral
plant but, as Goethe wrote in 1827, ‘the archetypal phenomenon . . . is
to be seen as a fundamental appearance within which the manifold is
to be held’. The Urpflanze was therefore a conjectural concept which
allowed hypothetical situations to be visualised.
Goethe’s botanical studies began some time during his first years
in Weimar in the late 1770s, and in 1790 he published his Versuch die
Metamorphose der Pflanzen zu erklären. This was his attempt to provide a
theory of plant morphology, and it was based upon his observations
of the serial homology of cotyledons, leaves and floral parts. Although
other botanists at the time were thinking along similar lines, it was
Goethe who clearly recognised that homology involves developmental
processes. His views on developmental integration and its potential
for evolutionary studies far exceeded that of Darwin although, owing
to the magnitude of the task, he was never able to apply his method-
ology to a wider plant world. Goethe was also the first to coin the
term ‘morphology’. He can rightly be described as the originator of
a phenomenological approach to botany and the father of compara-
tive morphology of plants. He subsequently influenced the develop-
ment of Gestalt Theory and theories of ‘self-organisation’, which are
of relevance to plant systematics and plant development respectively.
388 KNOWING PLANTS
were highly significant in their own right, and had an originality that
is now being increasingly realised.
The analysis of patterns of geographic distribution were central to
Wallace’s ideas on evolutionary theory, much of which was brought to
focus during his eight years in the Malay Archipelago (1854--62), but it
is not clear as to the importance he attributed to sympatric speciation
which is implicit in the above quotations from his 1855 essay. The
insular nature of the Malay Archipelago was to impress on Wallace
even more the factors that determine the boundaries of a species’
range. This was particularly the case for the fauna of the region,
which show affinities with both Asia and Australia. Wallace drew
attention to the sharp faunal boundaries between Asia and Australia
and the demarcation line separating the two great faunal regions
has come to be known as Wallace’s Line. We now know that this is
the result of the tectonic history of the region and that Wallace’s
Line coincides roughly with the position of the continental shelf of
Sundaland.
Although various ideas about movement of the continents had
existed since the time of Francis Bacon, during the mid nineteenth
century the continents were generally thought of as being static and
fixed. A well-formulated theory of continental drift was almost half a
century in the future. This led to concepts of floristic regions being
largely coincident with the major continental areas of the world, and,
of course, the corollary of static continents is dispersalism.
Darwin’s main postulates concerning plant geography were that
plants have achieved their present distributions through dispersal
from a centre of origin. These postulates also apply to species with
vicariant or discontinuous distribution patterns where the popula-
tions of a species are no longer in contact. Such dispersal could
be achieved by gradual spread through contiguous land masses or
by chance migration across natural barriers such as mountains or
oceans. Apart from the possiblity of polytopic origin, particularly as
a result of polyploidy, these postulates seemed reasonable and have
generally been accepted by the botanical community, but confusion
still remains about the proximate ability of a plant to disperse locally
and its ultimate ability to colonise globally. Many botanists believe
that, in orthodox biogeographic theory, there is a strong but naive
bias towards the immediate means of dispersal rather than the ability
of a plant to be part of a dynamic plant community.
Sir Joseph Dalton Hooker, who was a friend of Darwin, was
highly influential in British botany from the mid nineteenth century
onward. He originally favoured a land-bridge hypothesis to explain the
distribution of plants in the Southern Hemisphere but later, although
swayed by dispersalist hypotheses, he became sceptical about the
truth of both explanations. Darwin was extremely suspicious of land-
bridge theories and continental movements. He believed that the
explanation of a plant’s distribution was to be sought particularly
in its past history with respect to climatic change and the plant’s
powers of migration and survival, that is, in its ecology.
8.2 EVOLUTIONARY BOTANY 395
by the concepts that he used to frame his observations. His use of the
terms heredity and inheritance was based on a metaphorical extension
of the inheritance of property in human society, and therefore misrep-
resents biological reproduction. His concept of homology is derived
from the perspective of ‘property’ (the parts of an organism) being
inherited. Homology was to be determined through descent from a
common ancestor. Therefore, it is not surprising that some of his
most compelling arguments come from animal behaviour such as
competition for food and mates, territorial defence and from sexual
selection.
Competition between plants is not as obvious as between animals
and there is no real equivalent to animal behaviour. The analogue of
behaviour in the plant world is growth. The majority of plants dis-
play some degree of phenotypic plasticity, which tends to be optimal
for any given microhabitat. Phenotypic plasticity is the change in the
expressed phenotype of a genotype as a function of the environment.
However, there are many plants that have a relatively fixed develop-
mental pattern and do not exhibit much plasticity. In such cases the
norm of reaction is not expressed so much by the individual as by
the genome and so selection on plasticity can occur only through
selection in structured populations.
This highlights the great difference between natural selection in
the animal world where phenotypic plasticity is manifested more in
behaviour than in morphology. Had Darwin focused on plants earlier
he might have given additional weight to the reciprocal relationship
with the environment and its harmonising effects on the whole plant.
However, in the absence of a theory of heredity, such a course would
have brought him dangerously close to Lamarckism and, in any case,
plants would have provided little in the way of popular appeal for his
theory of natural selection.
Very few unequivocal examples of natural selection have been
observed in nature, most of the evidence for natural selection being
inferential, based of comparative data. It is difficult to perform evo-
lutionary experiments because of the timescales involved between
generations and that is why rapidly reproducing organisms such as
bacteria, Drosophila and Arabidopsis have been chosen by researchers.
But in most instances evolution must be inferred from observations
and such inferences must be tested against subsequent observations.
The study of adaptation is equally difficult, because the unit of selec-
tion is not a single character but the whole individual, the sum of all
its adaptations. Adaptation is therefore relative. If it were not so, then
organisms could not evolve or become extinct. It is a dynamic con-
cept stressing the changing environmental parameters and a species
response to them.
There are problems in the use of the words ‘adaptation’ and some
see mechanistic connotations in its use. Sometimes adaptation is used
in a physiological or sensory context when it then has a different
meaning. In an evolutionary sense, as it is used throughout this book,
many writers have noted its ambiguity. It is said to be non-scientific
398 KNOWING PLANTS
of plan’, for example the fins of whales and fishes. During the first
half of the nineteenth century the analogous similarities of organ-
isms, such as the zygomorphic flowers of mints and foxgloves, were
regarded as being the result of similarity of function alone, and not of
historical contingency or convergent evolution. Homologous similari-
ties were part of the plan of creation and were to be found also in the
correlation of parts, and this blinded Cuvier to the possibility of evo-
lutionary change. In the great debates of Cuvier and Geoffroy Saint-
Hilaire it is clear that neither were really asking the right question;
that is, what is the reciprocal relationship of the organism and its
environment? As a result Cuvier insisted that function determines
structure whereas for Geoffroy it was the other way round.
Darwin simply side-stepped the difficulty of interpretation by
declaring that all similarity is the result of proximity of descent from
the nearest common ancestor, and that analogous similarity is caused
by modification over time due to similarity of function. The time
dimension, plus, of course, the mechanism of natural selection, was
the crucial component missing in the theological viewpoint. Thus,
history was firmly re-instated as a fundamental factor of enquiry into
Nature.
During the nineteenth century the study of embryogenesis and
development was mostly focused on animals and this, in turn influ-
enced their classification. The classification of plants was probably
less influenced by evolutionary theory than that of animals, although
the maturation of an organism at different stages its development
(ontogeny) has been an important process in the evolution of plants.
When a plant reproduces at an earlier, more immature stage, it is
an example of paedomorphosis. Delayed reproduction or retardation
is less common in plants. Both phenomena have not been given the
prominence they deserve. According to Schleiden, Robert Brown was
the first to see that the history of development is the leading principle
in understanding the morphology and nature of plants. Others who
contributed greatly to the comparative embryology of plants within
an evolutionary context include the great plant anatomists of the
late nineteenth century such as Hofmeister, Strasburger, Goebel and
Bower.
The first comprehensive theory to explain differences in develop-
ment among organisms was the idea of ‘recapitulation’, which was
first proposed by the German Nature-philosophers. This idea had its
roots in the Scala Naturae of previous centuries, and its basic tenet is
that nature proceeds in steps from the simple to the complex, with
each organism passing through ancestral stages during its develop-
ment. The now (in)famous ‘biogenetic law’, that ontogeny recapit-
ulates phylogeny, was formerly proposed by Ernst Haeckel in 1866
and who modified the original recapitulation idea by suggesting that
the whole process involved changes in developmental timing, or hete-
rochrony. It was an appealing, if deceptively parsimonious hypothesis.
Some 40 years earlier, the theory of recapitulation had, in fact, been
challenged by K. E. von Baer (1792--1876), who argued that each stage
400 KNOWING PLANTS
8.3.5 Speciation
Speciation, from Darwin onwards, was one of the most fundamental
problems of evolution. Although Darwin and Wallace never actually
subscribed to the idea that geographical isolation was a precursor to
reproductive isolation and speciation, Mayr declared that the ‘mod-
ern synthesis’ was clearly only the maturation of Darwin’s theory of
evolution. They obviously saw the importance of islands in the speci-
ation process, but did not go as far as Mayr in elevating geographical
isolation as the major determining factor. By 1859 Darwin was ready
to accept sympatric speciation for many continental species due to eco-
logical isolation. Reproductive isolation is achieved in plants by many
different mechanisms. Mayr clearly recognised that the actual mecha-
nism of speciation ultimately resided in the genes and chromosomes.
Nowadays, the role played by internal factors such as polyploidy and
genetic turnover has to be addressed in any theory of plant evolu-
tion. Polyploidy, for example, is widespread in the angiosperms, and
current research is revealing that the plant genome is a dynamic
evolving system (see Figure 8.15). Several plant families such as the
Campanulaceae have massively rearranged chloroplast genomes in all
the major genera, the significance of which has yet to be realised.
Mayr’s Biological Species Concept (BSC) emphasises the reproduc-
tive isolation of species. The compelling attraction of the BSC is the
fact that it provides biological criteria for the recognition of some
of the discontinuity that exists in nature. The BSC places the species
as the basic unit of evolutionary biology, and as more natural than
higher categories. However, if time were somehow speeded up, we
might observe species becoming and disappearing in rapid succes-
sion, dissolving into one another, and into genera, just as we observe
the transient passage of individuals within generations. In a sense,
over evolutionary time, the species is no more real than any other
taxonomic category, and one can understand why the Nominalistic
Species Concept remained favourable among some botanists. How-
ever, functionally, the species has an importance not found in collec-
tive higher categories.
Mayr applied his BSC concept to a local flora in northeast United
States and concluded that an overwhelming majority of the species
could be embraced perfectly adequately within this concept. However,
in botany, the BSC has never been popular, and for most botanists,
particularly herbarium workers, a taxonomic (morphological or phe-
Figure 8.15. An example of netic) species concept was preferred. This has had at least one unfor-
sympatric speciation following tunate consequence for botany: diverse phenotypes, often of a single
hybridisation and polyploidy is the species or ploidy level, and often based on a single collection, have
evolution of Senecio cambrensis as been given specific status, thus burdening the nomenclature with
an allopolyploid derivative of a
superfluous names, and hindering subsequent investigation.
hybrid between S. squalidus and
S. vulgaris.
However, the most obvious reasons for the preference for a taxo-
nomic species concept in botany are as follows.
8.3 PHYLOGENY, GENETICS AND THE NEW SYSTEMATICS 409
Nature that exists today. The wider identification that may result from
such a transpersonal shift in psyche should allow for more empathy Deep Ecology – I could also call it
with, and a more spontaneous care for, plants and animals, instead ‘Green’ – the Green Movement is a
of treating them as commodities. It may also lead to a more rever- movement where you not only do
ential approach to Nature and a greater sense of ecoliteracy, which, good for the planet for the sake of
fortunately, can still be found in small, self-sustaining communities humans but also for the sake of the
worldwide. planet itself. That’s to say that you
start from the whole of the globe
However, there are also progressive and liberating aspects to
and talk about the ecosystems,
modernity, and there is a danger that, in our angst over ecologi-
trying to keep them healthy as a
cal catastrophes, we fail to appreciate the benefits that modernity value in itself. That is to say, for their
has brought. A re-enchantment of the world is not inconsistent with own sake, like you do things for your
aspects of contemporary science, and it would be unrealistic to turn own children or for your own dog,
the clock back. But the progress to a more ecoliterate society could not only thinking of the dog as an
involve a synthesis of both old and new values, and a realisation of instrument for your pleasure. So,
what we have already lost. We need balance and the skill to make the deep ecology starts from a
right decisions, but these can only come about by a new sensitivity philosophical or religious view that
all living beings have value in
to our place in nature.
themselves and therefore need
And what of botany? There is so much information coming at us
protection against the destruction
that we are in severe danger of overload. Information has now become from billions of humans.
a worldwide commodity, but are we able to synthesise it into a mean- Arne Naess (Nancho Rep: W. David
ingful programme? A four-year university course is hardly adequate to Kubiak, http://www.nancho.
provide a proper basis for twentyfirst-century botany. General botany, net/advisors/anaess.html)
including field and descriptive botany, is no longer taught, and the
history of botany is completely ignored, while systematic and taxo-
nomic research is now virtually the province of the molecular expert,
leaving the gifted amateur with almost no influence whatsoever on
how we should interpret the botanical world. Systematics is domi-
nated today by molecular biology and cladistics. Ph.D. theses are pro-
duced, ostensibly about plant evolution, but often with scarcely any
reference to the plant living in Nature, while botanical journals have
become dense and boring, filled with papers on molecular research. The highest that man can attain in
Too much taxonomic research consists of a seemingly endless com- these matters is wonder; if the
parison of cladograms produced by different molecular and analytical primary phenomenon causes this,
methods; and the search for the phylogenetic utility of the classifica- let him be satisfied
tions that are derived from the cladograms is inward looking, almost Goethe
forgetting the plants themselves.
This rather depressing picture does not give much optimism for
an ecologically enlightened future generation. Perhaps the idea of
formal university training in botany is just a hangover from an
outmoded modernity programme, and we need new ways of re-
enchanting botany. One of the finest examples of an inspiring alterna-
tive botany can be found in the work of the French botanist, Francis
Hallé, but this reflects a lifetime of experience that is rare in the
university lecture theatre. Yet, it may be timely to re-examine the
world of past botanists and possibly learn what they had to teach.
One approach that may prove richly rewarding is the ‘delicate empiri-
cism’ developed by Goethe and subsequently practised by Agnes Arber.
The phenomenological approach to botany allows for the dynamic
interplay between observer and the observed, a fertile ground for the
424 KNOWING PLANTS
Abram, D. The Spell of the Sensuous (New York: Vintage Books, 1996).
Arber, A. The Natural Philosophy of Plant Form, Facsimile edition (1970) (Darien,
CN: Hafner Publishing Co., 1950).
Berry, W. Life is a Miracle. An Essay Against Modern Superstition (Washington,
D.C.: Counterpoint, 2000).
Bortoft, H. The Wholeness of Nature (New York: Lindisfarne Books, 1996).
Brandon, R. N. Concepts and Methods in Evolutionary Biology (Cambridge:
Cambridge University Press, 1996).
Capra, F. The Web of Life. A New Scientific Understanding of Living Systems (New
York: Anchor Books/Doubleday, 1996).
Creath, R. and Maienschein, J. (editors) Biology and Epistemology (Cambridge:
Cambridge University Press, 2000).
FURTHER READING FOR CHAPTER 8 425
ABA see abscissic acid algae 49 animals differences from plants 49,
Abies 218, 336 colonial 40--41 52
abscissic acid 77, 78, 264 coenocytic or siphonous 39--40 anisogamy 29--30
abscission 58, 103 filamentous 41--43 anisophylly 68
Absinthe see Artemisia absinthum groups of 34--35 anisospory 145
Abutilon, nectar 171 intertidal 45 ANITA group 224
Acacia 103, 242, 272, 285, 298, 338 multicellular 38--39 annatto see Bixa orellana
phyllodes 126 unicellular 36--37 Annonaceae 173
Acanthaceae 247, 286, 288 Alismatales 231, 254 annual see life-forms
Acanthus as a mangrove species allele 29 annulus 142, 162
267 allelopathy 99, 159 Anothofixus 279
Acetabularia 38--39, 46 Alliaceae as vegetables 329 ant plants, ant-thorns 293, 299
development 93--94 allicin 341 Antheridium 137
Acetobacter 21 Allium 61, 223 Anthocerophyta, Anthocerotales,
Achillea, sneezewort 352 allometric growth 106--107 hornworts 198--199
Acorus 230, 254, 350 Alluaudia place in phylogeny 195
Acrostichum 267 Alnus 243, 255 Anthoceros 143, 199
Actinidiaceae 246 catkins 161 anthocyanadins 175, 176
Actinomorphy see flower symmetry Alocasia 180 anticlinal cell division 42
Adanson, M. 384 Aloe 185, 232, 301--302, 232, 314 Antirrhinum 91, 418
Adansonia 186, 303 Aloeaceae 185 Apiaceae, Apiales 249, 339
adaptation 99, 396--398, 410 Alsomitra 164 apical dominance 76
adaptive landscape 119 alternation of generations 31--32, apical meristem 64, 127
adaptive radiation 313--314 136 Apiopetalum 313
Adenium 303 Amaranthaceae 238--239 Apocyanaceae 246, 289, 303
adventitious roots 158 leaf venation 84 Apoideae 249
Aegialitis 267 pigments 176 apomorphy 416
vivipary 165 Amborella, Amborellaceae 227, 312 Aponogeton 165
Aegiceras 267 Ambrosia maritima ragweed 342 apophysis 142, 143
Aegle marmelos, Bael Tree 343 Ammophila, marram grass 160, 297 apoplasm 78
Aeonium 313 Amorphophallus 180, 186 apostasioideae 233
Aerenchyma 56, 259 Ampelodesmus 235 apple see Malus
Aeschynanthus 278, 313--314 Amyema 279 aquatic plants, general adaptations
Aeschynomene 258 Anabaena 18, 41, 212, 257, 273 254--257
Aesculus 187 Anacamptis 233 Aquifoliaceae 248
Aextoxicon 239 Anacardium occidentale 331 Aquilegia 185
Agalmyla 313 Anacyclus pyrethrum, white pellitory as Arabidopsis 81
agar 21 snuff 352 Araceae 175, 290
Agathis 218, 220, 311--313 Anadenanthera peregrine 355 Araliaceae 249
Agavaceae 169 Ananas pineapple 173, 332, 335 Araucaria 116, 218, 312--313
Agave sisalina, sisal 335, 345 Anarcardiaceae 245 island endemics 311
Agave tequilana 349 Andopogon 297 male gametophyte 153
Aggregate fruit 329 Andreaea protonema 138 regular branching 76
Aglaophyton 203 Andreaeopsida, stone or lantern Araucariales, Araucariaceae 220
air plants 234, 235 mosses 201 Arber, A. 371, 387, 412, 414--415, 423
Aizoaceae 238--239, 263 place in phylogeny 195 Arbutus 172, 270
Alchemilla 150 anemochory, see seeds, dispersal Arceuthobium 279
alcohol, production of 349 Angiopteris 208 archaebacteria 13, 19--22, 49
Aleurites, Tung Nuts 326, 337 Angraecum sesquipedale 171 Archaeopteris 125, 207
INDEX 427
Brassicaceae, Brassicales 149, 244 Calamus 288, 289 cassava see Manihot
as crops 318, 326--329 see also Acorus calamus Cassia 242
lack of mycorrhizae 270 Calceolaria, Calceolariaceae 172, 247 Cassytha 276, 277
brassinosteroid 78 California nutmeg 221 castor oil plant see Ricinis
Braun--Blanquet vegetation Calliandra 179 Casuarina, Casuarinaceae 243--244,
classification 406 Callistemon 185 270, 273, 279
breadfruiut see Artocarpus altilis Callitriche 255, 418 Catharanthus roseus 344--345
breeding systems 186 Calluna 184, 246, 270 Caulerpa 40
Brighamia 316 calmodulin 81 cauliflory 186
Bromeliaceae 185, 234, 288 Calobryales 197 Caytonia 149, 215
Brongniart, A. and A.-T. 389 Calvin cycle 16, 17 Cecropia seedling germination 158
brood place flowers 168 Calycanthus 180, 181 Cedrus 130
Broussonetia papyrifera, paper CAM see Crassulacean Acid Ceiba 186
mulberry 162, 335 Metabolism Celastrales 241
brown algae, see Phaeophyceae cambium, bifacial 207 cells 20--30
Brown, R. 390, 399 Camellia 245 complex 19
Brugmansia 247, 355 Camellia sinensis, tea 347 determination 81
Bruguiera 267 Camerarius, R. J. 381 division 22, 30
Brunoniaceae 250 Campanula, Campanulaceae 188, 315 membrane 21, 58
brush blossom 179, 185 Campnosperma 157 signaling 75, 78--79
Bryidae, arthrodontous mosses 202 Canacomyrica 313 size 21--22
Bryophyta, Bryopsida, mosses 199--201 Canada balsam see Abies types, cell wall 20, 57--59, 66
adaptation 31, 47, 126, 138--142, canalization 405 cellulose 21--23, 58
160--163, 294--295, 299 Canarina canariensis 315 in paper-making 335
phylogeny 195, 196 canellales 229 Celmisia 304
Bryopsis 40 Candolle, A. de 388--390, 395, 402 Centaurea 250
Bryum 162, 202 Canna 178, 236 centriole 26
Bubbia 173 Cannabidaceae 243, 326 Centropogon 175
Buch, L. von 395 Cannabis 60, 334, 353 Centrospermae see Caryophyllaceae
buckwheat see Fagopyrum esculentum Cannaceae 236 Cephalotaceae 279
bud 62, 67, 68 canola see oilseed crops Cephalotaxus 143
Buddleja 183 cantharophily see beetle pollination Cephalotus 241
Buffon G. L. L. 389, 395 Canthium 313 Cephaloza, spore dispersal 162
bulbil 61, 62 capitulum structure 249, 250 Ceratonia 337
Bulbophyllum 61, 178 Capparis 179 Ceratophyllum Ceratophyllales 166,
Burmanniaceae 231 Caprifoliaceae 248 254, 256
Burseraceae 245 capsaicin 341 Ceratopteris 260
Busbecq, G. 363 Capsella embryogenesis 156 Cercidiphyllaceae 239
Butomaceae 231 Capsicum 341 cereal crops 318, 321
Butomus 230 capsule 142 Ceropegia 180--181
butterfly and moth pollination 183 Caralluma 300, 302 Cesalpinioideae 242
Buxbaumia 140 carbon fixation 9, 18 Cesalpino, A. 378, 381
buzz pollination 182 cardamon see Elettaria cardomomum Chaetomorpha 42
Byblidaceae 279 Carex 235 Chaleuria 145
Caricaceae 244 Chamaecyparis foliage 110
C3 plants 282 Carnegia gigantea 303 Chamaelium, chamomile as snuff 352
C4 plants 282 carnivorous plants 279--280 Chamaephyte see life-forms
Cabomba Cabombaceae 228, 259, carob see Ceratonia Chara, Charophyceae, Charales 32, 43,
260 carotenoid 10--11 47--48, 137, 257
Cactaceae, cactus 103, 238, 290, carpel 149 chemical evolution of the Earth 2
300--303 Carpinus winged fruit 163, 164 chemical repellants and deterrants
Cakile 260, 264 carragheen 21 249, 251
Calamites 209 Caryophyllaceae 238 chemoton 6
Calamostachys 145 cashew nut see Anacardium occidentale Chenopodiaceae 176, 238--239
INDEX 429
Cynodon dactylon, Bermuda grass 297 dicliny, diclinous 188 ebena stuff 355
Cyperaceae 234--235, 255, 270 Dicnemon gametophyte 139 ebony see Diospyros
Cyphostemma 239 Dicranella 202 Ecbalium, seed dispersal 163
Cyprepedioideae 233 Didiereaceae 238, 301 Echeveria 239
Cypripedium, Lady’s Slipper Orchid differentiation 57, 89 Echinocactus 301
179 Digitalis 248, 418 Echinops 250
Cypress see Cupressus Digitaria 324 Echium 307, 313, 314, 315
Cyrillaceae 246 Dillenidae 244 ecology 395, 406, 410, 421--422
Cyrtandra 314 Dinobryon 36 ectocarpales 44
Cytinus 275 Dinochloa 288 egg cell, ovum 137
Cytisus 180, 181 dinophyta, dinoflagellate 23, 35--36 Eichler, A. W. 402
cytokinesis 27, 28 diocles 375 Eigen, M. 4
cytokinins 77 dioecy 30, 145, 187--188 Elaeis guineensis 320
cytoskeleton 23, 27, 28 Dionaea 99, 280 Elaeocarpus 313
Dionocophyllaceae 279 elaiosome see oil bodies
D’Arcy Thompson, W. 110, 400 Dioscorea, Dioscoreaceae, Dioscoreales, elater 141, 162
Dacrycarpus 218 231, 327--328, 345 electron transport 13
Dahlgren, B. E. 418 Dioscorides 342--343 Elettaria cardomomum 340
Dalbergia, rosewood 333 Diospyros ebony 313, 333 Elizabetha princeps 355
Dalechampia 173 diplobiontic see life-cycle Elodea 63, 166
Darlingtonia 246, 281 diploidy 29, 33--34 Embryobionta, Embryophyta, plants,
Darwin, E. 389 Diplophyllum 142 land plants 28, 36, 46--53, 195
Darwin, C. 97--98, 107, 388, 391--395, Dipsacaceae 248 embryogenesis 156
399--401 Dipteridiales 210, 211 embryosac 152
Dasycladales 46, 93 Dipterocarpaceae 244 Empetrum hermaphroditum 306
date palm see Phoenix Dischidia 293 Encelia allelopathy 159
Datura 172, 355 dispersal 31, 135--136, 140, 157--170 Encephalartos 156, 217
Dawsonia 201 distichous arrangement 68, 129 endemic plants 308--313, 369
Decaspermum 187 DNA 6 endocytosis 24
decumbent 68 sequencing 419 endosperm 149
Degeneria, Degenericeae 312 doctrine of signatures 344 Endospermum 157
Deherainia 184 Dodecathon 245 endospory 146
Delissea 316 Dokuchaev N. N. 395 endosymbiont, endosymbiosis 24--26
Delonix 242 domains of life 21, 22 Engler, A. 402
deme 409 domestication of crop plants 318 Enhalus 260
Dendroceros 199 double cocoanut see Lodoicea Entada gigas hydrochory 165
Dendrophatae 278 Douglas, David 365 Enteromorpha 48
Dendrosenecio 307 Dracaena 312 environment 97, 98
Dendroseris 315 Dracophyllum 307 Ephedra 222, 345
Dendrotrophe 278 Drakea 181 ephemerals 300, 301
Dennstaedtia 214 Draparnaldia 42 Ephemerum 202
Derrbesia 47 Driesch, H. 400 epicotyl 62
Descartes, René 379 Drimys 229 Epidendrum 178, 392
Deschampsia klossii 307 drip-tip 285, 295 epidermis 84--85
Desmarestia life-cycle 32 Drosera Droseraceae 239, 279, 282 epigenetics 87--91
desmid 37 drought, response to 103 Epilobium 164
determinate growth 89 drupe 329 epiphyte, diversity and adaptations
development 56--61, 70, 75, 110, Dryandra 270 286--294
116 Dryas octopetala 98 Episcia 288
Dianella 313 Drynaria 290 Epulipiscum 21
diaspore 157 Dryopteris 63, 137--138, 141--143 Equisetum Equisetopsida, horsetails
diatom see Bacillariophyceae Dubautia menziesii 307--308 85, 106, 138, 140, 143, 195,
Dichondra 247 durra see Sorghum 209
Dicksonia 213, 313 dyes 337 Eremoplepidaceae 277--278
INDEX 431
Erica, Ericacaee, Ericales 152, 168, Ferocactus 301 gametophyte 31--32, 138--140, 146--147,
245--246, 270--271, 290 ferredoxin 12 152--153
Eriocaulaceae 235 fertilisation 144, 155 Ganti, T. 6
erucic acid 326 Ferula (Apiaceae) 338 garden history 360
Eryngium 249, 314 Festuca, Fescue 62, 298, 307, 325 Garner and Allard 102
Erythroxylon coca 354 Fibonacci angle 127--128 Garrya, Garryales 246
Espeletia 307, 314 fibre 60 Gaza, T. 377
essential oils 339 Ficus 169--170, 173, 288--290 gelatinous fibres 102
ethanol 349 fig, see Ficus gemmae 160
ethylene 77 Filipendula 150, 345 gene regulation of development see
eubacteria 18--22, 49 Fisher, R. A. 406 epigenetics
Eucalyptus 74, 185, 241, 291, 334--337 Fissidens 202 genetic drift 29
Eucalyptus citriodora, as source of flagellum(a) 26--27, 31, 36 genetic manipulation of crops
citronella 337 flavonoids 168 359--360
Euchema 21 flavourings 340--341 genetic repair 29--30
eudicots 237, 240 flax see Linum genetics, influence of 405
Eudorina 41 Fleur de Lis see Iris Genlisea 281
Eugenia caryophyllus 340 florets in Asteraceae 250 genome 5
eugenol 356 flower form (architecture, colour, genotype 33, 116--117, 121
Euglenophyta, euglenoids 34--36, patterning, symmetry) 174--179 Gentiana, Gentianaceae 246
46 advertising 173 Gentianella 117
Eukarya, eukaryotes 19--27, 34, 49 development, ABC model 92--93 geological periods 53
eumagnoliid 229 pollination 175, 182--184 geophyte/cryptophyte see life-forms
Euonymus 241 flower symbolism 360 geotropism 98
Euphorbia, Euphorbiaceae flowering plants see Magnoliopsida geraniol 356
Euphorbiales 173, 188, 241, flypaper traps 280 Geranium, Geraniaceae, Geraniales
300--302, 326, 327 Foeniculum vulgare fennel 351, 362 240, 307--308
Euphrasia 177, 276 follicle 149--150 Gesner, C. 378--379
Euphyllophytina euphyllophytes 195, Fonio see Digitaria Gesneriaceae 247, 290
203, 206--207 Fontinalis 63, 202 Gestalten 413
Eupomatia Eupomataceae 173, 312 food body 173 Ghini, L. 378
eusporangium 141--142 Ford, E. B. 406 gibberellins 66, 77, 87
Eustigmatophyceae 36 Fouqueria Fouqueriaceae 303 Gimour, J. 350
Everglades 256 Fragaria 150 ginger see Zingiber
evolution 112--113, 406 Frankenia, Frankeniaceae 238, Ginkgo Ginkgoidae maidenhair tree
Excoecaria 255 264 83, 137, 153, 155, 195, 217
exfoliation 74--75 Frankia 243 ginseng, see Panax
exons 7 Franklinia 313 Glaucocystis 36
Exospermum 173 Fremontodendron 313 Glaucophyta, Glaucocystophyta 25,
explosive fruit see autochory Freycinetia 185, 288--290 35--36
extinction, rates on islands 308 Fritillaria 176--177 Glaux 264
Fritschiella 42, 138 Glechoma hederacea 187, 352
Fabaceae, Fabales 161, 179, 242, 272, fruits 149, 173, 329 Gleicheniales 210, 211
326 Frullania 196 Glochidia 104
Faboideae 242 Fucus, Fucales 32, 44 Gloeochaete 36
Fagus, Fagaceae, Fagales 161, 243--244 fuel plants 338 Gloger, C. W. L. 396
Fagopyrum esculentum 325 Fumarioideae 237 glucosinolate distribution 244, 326
Fagraea 290 fungi 49, 51 Glycine max 325
Fairchild, T. 380 fynbos 269 Glycyrrhiza glabra, source of liquorice
favism 325 345, 351
feedback loops 108, see also hypercycle Galactites 250 GM crops 359--360, 421
fen succession see hydrosere galactose 21 Gmelinin, S. G. 384
Fennel, see Foeniculum vulgare Galeola 274 Gnetum Gnetidae, gentophytes 73, 83,
fern see Polypodiopsida Galvezia speciosa 310 148, 195, 222
432 INDEX
Goethe, J. W. von 99, 129, 387--388, Haptophyta see Prymnesiophyta Hooker, J. D. 388, 365, 394--395, 402,
423 hardwoods 333 404
archetypes 413--414 Hardy--Weinberg equilibrium 34, 406 hopeful monster 412
Goldschmidt, R. 412 harmony 373 hops see Humulus
Gonium 40--41 Hartig Net mycorrhizae see Hordeum vulgare, for alcohol 349
Goodeniaceae mycorrhiza hormones see plant growth
Goodwin, B. 93--95 haustorium, in parasitic plant compounds
Gossypium 174, 335--336 275--276 Horneophyton 203
Gould S. J. 107 heathland 269 horticultural traditions 367
Gram positive bacteria 20 Hebe 304, 314, 418 Hottonia palustris 259
Gram, Christian 20 hedgehog plant 305 Humboldt, A. von 388
grapes see Vitis Hedwig, J. 384 humulone 341
Grass see Poaceae Hegel, G. 386--387 Humulus 187, 350
grassland 295--297, 324--325 Heliamphora 246, 281 Hura 344
gravitropism 101 Helianthus annua, sunflower 327 Hutchinson, J. 418
Gray, A. 395, 404 Helichrysum 249 Huxley T. H. 112
green algae see Chlorophyta Heliconia 236 Hyacinthoides 62
green non-sulphur bacteria 13 Heliobacterium Heliobacteriaceae 13--15 hybridisation, 409--410
green plants see Embryophyta Helleborus, honey leaves, nectar 171 hydathode 257
green revolution 421 helophyte, marsh plants see life-forms Hydnocarpus kurzii, source of
green sulphur bacteria 14 Helwingia 248 Chaulmoogra oil 345
Grevillea 185 hemp 334, see also Cannabis Hydrangea 245
Grew, N. 380 henna see Lawsonia inermis Hydrasperma 147
Grisebach, A. 395 Hennig, W. 414, 416 Hydrilla 165
Grossulariaceae 239 Heracleum 249 Hydrocharis, Hydrocharitaceae 62, 231
ground meristem 65 Heraclitus 373 Hydrocotyle, Hydrocotyloideae 249
growth 69 herbaceous vegetation 160 hydrocyanic acid HCN 328
Grypania 22, 39 herbalism 374--375, 378 Hydrodictyon 40
Guaiacum officinale 333 Herberta 196 hydrophyte, aquatic plant see life
guerilla growth 159 herbivory, defences against 298--299 forms
gum trees see Eucalyptus herbs 338 hydrosere 255
Gunflint Rock Formation Canada heroin 353 Hymenophyllales 210--211
38--39 Hesperidium 329, 330 Hyoscyamus niger 344
Gunnera 273 Hesperoromannia 316 hypanthium 243
gutta percha see Palaquium gutta Heterachaenia 313 hyper- and ultra-epiphyte 290
guttation 257 heteroblastic development 110 hypercycle 4
gymnosperm 215 Heterochaenia 313 Hypericum 168, 169, 241
heteromorphy 32 hyperpachycaul 314--315
Haeckel, E. 110, 399, 414 heterospory 145, 164 Hypnum 202
Haldane, J. B. S. 406 heterotroph 24 hypocotyls 62
Hales, S. 380 Hetrochaenia 315 Hypolepis 214
Halimeda 40 Hevea 241, 337
Halimione 265 Hibiscadelphus 316 IAA see auxins
Hallé, F. and Oldeman R. A. A. 130, Hibiscus kenaf fibre plant 179, 244, Ibn Sina 376
423 335 Iboga vine see Tabernanthe
Halophila 260 hierarchy see taxonomy ichthychory, fish dispersal 166
halophyte 260--262, 265 Himantandraceae 312 identity genes 89--92
Hammarbya 61 Hippuris 106, 418 idioblast 60, 61
hapaxanthic 130 historical contingency 397 Ilex 248, 347
haplobiontic and haplodiplobiontic Hofmeister, W. 391 Illicium 228, 351
see life-cycles holdfast 42, 45 Impatiens, seed dispersal 163
haploid 29 homeosis 412 indeterminate growth 90
Haplomitrium 197 homoiohydry 196 Indigofera 242, 337
Haplopappus canus 310 honey-guides see flower patterning indusium 143
INDEX 433
nitrogen fixation, in the rosids 240, origin of species 396, 402 Pediastrum 41
243, 271--272 ornithophily see bird pollination Pedicularis 276
node 62, 67, 69 Orobanche, Orobanchaceae 163, 248, Pelargonium 240
Nolanaceae 247 275--276 Pellia 137, 162, 198
nomenclatural rules 382 Orris root see Iris peloric flower 91
nominalism 377 orthostichy 128 Pelvetia 30
Nostoc 273 orthotropic axis 68 Pennisetum glaucum 324
Nothofagus 313 Oryza, rice 321, 322, 323 Pentaclethra 285
Notholaena parryi, resurrection fern Osbornia 267 Pentastemona 231
299 Oscillatoria 17 Pentstemon 418
Notothyllales, Notothylas 199 osmoregulators and osmoconformers Peperomia 313
nucellus, crassinucellate and 263 pepper see Piper
tenuinucellate 151--152 Osmunda Osmundales 142, 210 peppermint 339
nucleus 20, 22 ovule and seeds 147--148, 151--152, peptidoglycan 20
numerical taxonomy 416--417 215--216 perennial 90
Nuphar 165, 166, 228 as pollination attractants 168 Pereskia 104
nutmeg see Myristica fragrans ovum see egg cell perfume 356
nutrient conditions 269 Owen, R. 400 pericarp 149, 169
nuts 331 Oxalis, Oxalidales 61--62, 241 periclinal cell division 42
Nyctaginaceae 238 Pericopsis elata, afromosia 333
Nymphaea, Nympheaceae, Nympheales pachycaul 73 periderm see bark
91--92, 165--166, 228, 254, Pachypodium 303 peristome 162
258--260, 362 paedomorphosis 111 Pernod 351
Nypa fruticans 266, 318 Paeonia, Paeoniaceae 224, 239, 363 Persea americana, avocado 329
Palaeonitella 47 petals 224
Oak see Quercus Palaquium 246, 337 petiolode 114
Ochroma 186, 333 palisade layer 84 peyote see Lophophora
Ochrophyta 26, 35--37 palm see Arecaceae Phaeoceros 199
Ockham, W. 377 pampas grass see Cortaderia Phaeocystis 36
Oedogonium, life cycle 32 Panax ginseng 344 Phaeophyta, Phaeophyceae 30, 35, 37,
Oenanthe 260 Pancratium maritimum 260, 363 39, 43--44
oil bodies 172 Pandanus, Pandanaceae Pandanales phagocytosis 24
oilseed crops 326 185, 231, 255 phalanx growth 159
Oken, L. 386 Pandorina 41 Phalaris arundinacea 255
Olacaceae 239 Papaver Papaveroideae, Papaveraceae phanerophyte see life-forms
Olea europaea, Oleaceae, source of oil 237, 326, 353 phellem, see bark 73
247, 326--327, 360 paper making 335 phellogen, cork cambium 61
oligotrophy 256, 258 Papilionoideae 242 phenomenology 423
Onagraceae 241 pappus 163--164, 250 phenotype 33, 116--117
Oncidium 176, 233 Paracryphia 313 Philesiaceae 232
ontogenetic contingency 117 Paramecium 46 Philodendron 288
oogamy 29, 30 parasitic plants 275--277 Phlegmaria 204
oogonium 137 Parasponia 272 phloem 59, 65--66, 70
Ophioglossopsida, Adder’s-tongue and parastichy 128 Phoenix dactylifera 319
Moonworts 195, 208 parenchyma 58 Phormium tenax, New Zealand flax
Ophrys 174, 181 Parkinson, John 363 193
Opiliaceae 239 Parmenides 374 photomorphogenesis see
opium poppy see Papaver Parnassia 121 morphogenesis
Opuntia 303 Passiflora 179 photoreceptors 102
Orchid, Orchidaceae 163, 178, 190, Pastis 351 photosynthesis 8--16, 25, 36, 234, 238,
233, 274, 287, 291, 294 pattern formation 90 282
order 108 pattern, cell 86 Phragmipedium 233
organelle 19--20, 23, 25 pectic substances 58, 59 Phragmites australis 260
organisation, polarity 81--83 Pedaliaceae, source of oil 326 phragmoplast 28
436 INDEX
phycobilisome 18, 25, 36 plant growth, growth compounds 60, polysymmetry see flower symmetry
phycocyanin, phycocyanobilin, 77--78 Polytrichum Polytrichidae 126, 138, 201
phycobilin 10--12 Plantae, kingdom see Embryobionta pondweeds see Zannichelliaceae and
phycoerythrin 11--13 Plantago 263, 265, 418 Ruppiaceae
Phyllanthus embelici, Indian gooseberry plasmalemma see cells, membrane population genetics 406, 411
343 plasmodesmata 43, 58 Populus 255
Phyllites 214 plasticity 13, 117--119, 397 Posidonia Posidoniaceae 167, 231, 260
Phyllocladus 218, 220 plastid 24 Potamogeton 165--166, 257--260
Phylloglossum 204 Platanus 237 potatoes see Solanum tuberosum
phyllomorph 114 Plato’s Idealism 372--374 Potentilla 62
Phyllonoma 126--127, 248 Platycerium 214 Pottia 202
phyllotaxis 127--129 Platyzoma 145 Prantl, K. 402
Physoplexis 250 pleiotropism 106 prasinophyte 46
Physostigma venenosum, calabar pleonanthic 130 prebiotic Earth 1--2
345 plesiomorphy 416 Prigogene, Ilya 4
Phyteuma 109 pleurastrophyceae 47 primordium see apical meristem
phytochrome 10, 100 Pleurothallis 175 Primula, Primulaceae 189, 245
Phytolacaceae 238 Plicosepalus 278 Pringlea 315
phytosociology 406 plumbaginaceae 238 procambium 65
Picea 306, 333 pneumatophore 266 Prochloron Prochlorophytes 18
Picrorhiza kuroa, Kutki 343 Poa 298 procumbent 68
Pilularia 146, 212 Poaceae, grasses 85--86, 234--235 proembryo 156
Pimelea 304 for food 321 programmed cell death 56--57
Pine see Pinus grasslands and savanna 295--298 prokaryote 22, 24, 27, 49
pineapple see Ananas lack of mycorrhizae 270 prolepsis see growth
Pinguicula 282 Podocarpus Podocarpaceae proline 264
Pinopsida, gymnosperms, 195 Podocarpales 153, 220 promeristem 64, 69
Pinus, Pinales, Pinidae, conifers Podophyllum peltatum, source of protandry 188
143--144, 151--153, 164, 195, 215, etoposide, podophyllotoxin 345 Protea Proteaceae, Proteales 185--186,
218 Podostemaceae 255 237, 270
anatomy 63, 64, 74, 270 poikilohydry 196, 205 protoctista 49
pioneer species 157, 158 poisons, plants as a source of 344 protogyny 188
resins and timber 332--333, 336 polarity see organisation protonema 138, 139, 140
Piper methysticum, kava 347 Polemoniaceae 245 Protosiphon 39
Piper, pepper seedling germination pollard 62 protoxylem 65, 66, 70
158, 229, 290, 340, 343 pollen 143--144, 153--155, 168 Prunoideae 243
Pipturus 313 pollen flowers 168--169 Prunus 150, 188, 360
Pistacia 245 pollen sac 144, 152 Prymnesiophyta 35--36
Pistia 231, 257, 258 presentation in Asteraceae 250 pseudanthium 248
pistil 149 release, deposition and entrapment pseudocarp 330
Pitcher plants 281 161--164 Pseudoscourfeldia 46
pitfall traps 280 pollination flowering plants 153--155 Psilotum Psilotophytina Psilotopsida,
Pitocalyx 228 in aquatic plants 166, 167 whiskferns 63, 68, 195, 207--209
pits 43, 58, 60 buzz-pollination 168 psychoactive drugs 354--355
Pittosporum 313 syndromes 171, 181--186 psychophily see butterfly and moth
plagiotropic branching 68, 76, 129, pollinia 179, 183, 247 pollination
130 polyembryony 156 Psychotria 313
plant breeding and improvement Polyepis 307 Pteralyxia 316
356--360 Polygonaceae 125, 238, 270 Pteridium 214
plant disease 357--359 polyploidy 30, 251 Pteridium lateral spread, phalanx
plant form, concepts of 61, 105, 123, polypodiophytina 195, 208--214 growth 159
413 Polypodiopsida, Leptosporangiate Pterocarya 243
plant geography of Darwin and ferns 195, 209 Puccinellia 265
Wallace 393, 396 reproduction 137, 162 pulses 325
INDEX 437