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P o l l i n at i o n a n d F l o r a l E c o l o g y
This page intentionally left blank
P o l l i n at i o n a n d F l o r a l E c o l o g y

Pat Willmer

Princeton University Press

Princeton and Oxford
Copyright © 2011 by Princeton University Press
Published by Princeton University Press, 41 William Street,
Princeton, New Jersey 08540
In the United Kingdom: Princeton University Press, 6 Oxford Street,
Woodstock, Oxfordshire OX20 1TW
press.princeton.edu
Jacket photograph: The bee Eucera longicornis foraging on the sweet pea
Lathyrus. (c) Andrej Gogala

All Rights Reserved

Library of Congress Cataloging-in-Publication Data

Willmer, Pat, 1953-
Pollination and floral ecology / Pat Willmer.
    p. cm.
Includes bibliographical references.
ISBN 978-0-691-12861-0 (cloth : alk. paper) 1. Pollination. 2. Polli-
nation by insects. 3. Pollination by animals. 4. Plant ecology. I. Title.
QK926.W55 2011
571.8'642—dc22 2010049061

British Library Cataloging-in-Publication Data is available

This book has been composed in Times

Printed on acid-free paper ∞

Printed in the United States of America

10 9 8 7 6 5 4 3 2 1
 Contents

Preface vii
Acknowledgments ix

Part I Ess e nt i als of F low er D e si gn an d F unct i on

Chapter 1 Why Pollination Is Interesting 3

Chapter 2 Floral Design and Function 11
Chapter 3 Pollination, Mating, and Reproduction in Plants 55
Chapter 4 Evolution of Flowers, Pollination, and Plant Diversity 88

Part II F loral Ad ve rt i s e m ents an d F loral Re war d s

Chapter 5 Advertisements 1: Visual Signals and Floral Color 105

Chapter 6 Advertisements 2: Olfactory Signals 134
Chapter 7 Rewards 1: The Biology of Pollen 154
Chapter 8 Rewards 2: The Biology of Nectar 190
Chapter 9 Other Floral Rewards 221
Chapter 10 Rewards and Costs: The Environmental Economics of Pollination 234

Part III Poll i nat i on S yn d rom e s?

Chapter 11 Types of Flower Visitors: Syndromes, Constancy, and Effectiveness 261

Chapter 12 Generalist Flowers and Generalist Visitors 288
Chapter 13 Pollination by Flies 304
Chapter 14 Pollination by Butterflies and Moths 322
Chapter 15 Pollination by Birds 337
Chapter 16 Pollination by Bats 356
Chapter 17 Pollination by Nonflying Vertebrates and Other Oddities 370
Chapter 18 Pollination by Bees 378
Chapter 19 Wind and Water: Abiotic Pollination 418
Chapter 20 Syndromes and Webs: Specialists and Generalists 434
vi • Contents

Part I V F loral Ecology

Chapter 21 The Timing and Patterning of Flowering 483

Chapter 22 Living with Other Flowers: Competition and Pollination Ecology 503
Chapter 23 Cheating by Flowers: Cheating the Visitors and Cheating Other Flowers 524
Chapter 24 Flower Visitors as Cheats and the Plants’ Responses 542
Chapter 25 The Interactions of Pollination and Herbivory 554
Chapter 26 Pollination Using Florivores: From Brood Site Mutualism to
 Active Pollination 565
Chapter 27 Pollination in Different Habitats 575
Chapter 28 The Pollination of Crops 605
Chapter 29 The Global Pollination Crisis 620

Appendix 639
Glossary 643
References 663
Subject Index 751
Index of Animal Genera 768
Index of Plant Genera 771
 P r ef a c e

When I first became interested in pollination biology ers in the field: Jones and Little (1983) began the trend
around thirty years ago, there was essentially just one with Handbook of Experimental Pollination Ecology,
book to consult for core information, the classic by while Lloyd and Barrett (1996) produced Floral Biol-
Faegri and van der Pijl, The Principles of Pollination ogy: Studies on Floral Evolution in Animal Pollinated
Ecology, which has been the inspiration to genera- Systems, opening up a broader and more ecological
tions, its last edition appearing in 1979 but still struc- and evolutionary perspective on the whole subject.
tured around the 1966 original. But twenty years on I Then two collected contributions came along in 2006,
became frustrated that there had been no single vol- picking up the themes that had been emerging in the
ume since that date which covered the field. This is preceding decade: Waser and Ollerton in Plant-Polli-
particularly extraordinary given that the subject itself nator Interactions: From Specialization to General-
has expanded and blossomed prodigiously, both in its ization, and Harder and Barrett in Ecology and Evolu-
own right and as a testing ground for wider theories, as tion of Flowers. These have been seen as especially
well as having assumed greater importance in both sci- important in expounding new approaches and expos-
entific circles and as a wider public concern. ing older assumptions to a more critical analysis. The
It has not been all quiet on the publishing front debates about generalization and specialization, and
since the 1970s of course. There have been excellent the usefulness of the syndrome concept or of alterna-
books with more of a natural history approach (M. tive modeling approaches, have been particularly
Proctor et al. 1996; Buchmann and Nabhan 1996) and thought-provoking, so that anyone starting out as a re-
botanical books concentrating on floral structures searcher in pollination ecology will find much to en-
(Barth 1985; Endress 1994) or on floral development gage them from the authors represented in those two
(Glover 2007). Over the same period many extremely books.
useful edited volumes have also appeared, each with Those readers, however, would not get the back-
chapters contributed by experts updating readers on ground information, the core material of pollination
particular themes, such as nectar and nectaries (Bent- and floral biology. A beginner would still have to ex-
ley and Elias 1983; Nicolson et al. 2007), anthers and plore very widely across the mass of scientific jour-
pollen (D’Arcy and Keating 1996; Dafni et al. 2000), nals, hoping to light upon a reasonably up-to-date re-
and floral scents (Dudareva and Pichersky 2006). Sev- view article. And in the last decade the primary
eral books have compiled useful reviews on practical literature has undergone an extraordinary explosion in
techniques (Dafni 1992; Kearns and Inouye 1993; volume, almost more than in any other field, partly be-
Dafni et al. 2005) or on applied aspects of crop polli- cause of the practical and applied environmental prob-
nation (Free 1993), while Chittka and Thomson (2001) lems now seen to be emerging with pollination ser-
took a fresh approach by assembling chapters on as- vices, and partly because around twenty-five years ago
pects of pollinator cognition and learning. interest began to spread much more widely beyond the
But perhaps most important have been a select few European and North American temperate pollination
edited volumes with broader pollination coverage and systems, with expertise emerging especially in the
sometimes a more eclectic assemblage of contribu- New and Old World Tropics, in southern Africa and
tions. Here the editors have been very much the lead- Australia, and in Japan and China.
viii • Preface

For all these reasons, it seemed to me timely to at- those highly respected authors whose work I draw
tempt a book that would cover the subject more thor- heavily on. Some, seeing pollination biology as pio-
oughly, providing chapters on every key topic, and neering a new era where ecological modelers have
serve both as an introduction for anyone coming into more to tell us than old-style field workers, might
the field as advanced undergraduate or postgraduate find my approach too traditional. But at least those
and as a source book for professionals. Begun half coming in to the field hereafter may gain a better un-
way through the decade, it has inevitably burgeoned derstanding of the foundations on which models can
beyond the original intentions as the expanding litera- be built and so will better see where the key issues
ture burst around my ears, to the distress of my pub- may lie.
lishers. But the resulting book will, I hope, achieve at
least part of its aims and will not too greatly annoy Pat Willmer, November 2009
 A c k n o w l e d g me n t s

It is a pleasure to begin by thanking the many genera- Peter Gibbs, Aubrey Manning, Gidi Ne’eman, Sue Ni-
tions of students and postgraduates who have let me colson, Samy Zalat, Theodora Petanidou, Chris
know when I taught them in ways that inspired their O’Toole, and Rob Raguso.
interest and when I merely confused them. From Several of these colleagues have read and com-
them, I realized where the real fascinations of pollina- mented wisely on outlines, drafts, or chapters for me,
tion lay and where my own interests were too biased and to them I owe enormous gratitude and an apology
or quirky for a wider audience—I have tried, not al- where I have insufficiently taken on their criticisms;
ways successfully, to play down those quirks. Many the misconceptions or infelicities that remain are en-
former postgraduates and postdocs, now running re- tirely my fault. Particular thanks to Clive Nuttman on
search groups of their own and blossoming into major color and scent issues, Peter Gibbs on incompatibility
players in the world pollination and mutualism de- and on general issues of specialization and syndromes,
bates, have been especially important to me, and I Francis Gilbert (especially for updating my dipteran
thank them all for discussions, arguments, and the taxonomy), and Jonathan Pattrick for taking a broad
chance to read and learn from their own works; in par- beginner’s view of the book and being even more per-
ticular I must pay tribute to Graham Stone (GS) and snickety about semicolons than I am!
Simon Potts (SP), and more recently to Clive Nutt- I am deeply grateful to many who have allowed me
man (CN), Betsy Vulliamy, Gavin Ballantyne (GB), to use their photographs, which usually put my own
Caroline King, and Jonathan Pattrick, and to those efforts to shame. All are acknowledged by initials in
whose names are followed by initials for use of their the plates, and all of course retain their copyrights in
photos. the photos reproduced here. Susie Whiten (SW), Ali-
On a wider front, I confess to being a very poor son Fernie (AF), Ian Johnston (IJ), and Sandy Edwards
networker, so that I know the pollination biologists of (SE) were generous with their own photographs from
the world far less well on a personal level than I should, the UK and abroad. Special thanks to Steve Johnson
which is my loss. My communications with them have (SJ), Dino Martens (DM), Karen Sarkisyan (KS), and
nevertheless been wonderfully invigorating, and I Andrej Gogala (AG) for supplying superb photographs
thank so many of them for their generosity in exchang- of the more difficult animal visitors. I also owe a mas-
ing ideas. In particular, I have benefitted at various sive debt of gratitude to my illustrators, especially
times from conversations about bees or pollination or Dawn Toshack for most of the pictures of flowers and
wider mutualisms, whether prolonged or brief (and visitors and their detailed structures, and Caroline
some so brief they will scarcely remember me!), with King for reproducing most of the graphical figures
Jane Memmott, Steve Johnson, Judith Bronstein, Sally from other published works, as well as to Dimitri Kar-
Corbet, Florian Schiestl, Dick Southwood, Naomi etnikov for advice on figures in general. I must also
Pierce, Amots Dafni, Nigel Raine, Ingrid Williams, thank others at Princeton University Press who have
Cathy Kennedy, Francis Gilbert, Dino Martens, John patiently supported my efforts to complete this work;
Free, Jette Knudsen, James Cresswell, Steve Bullock, for the initial enthusiasm of Robert Kirk especially,
James Cook, Peter Yeo, Scott Armbruster, Mo Stanton, and the subsequent diligence of Stefani Wexler, Beth
Spencer Barrett, Dini Eisikowitch, Barbara Gemmill, Clevenger, Gail Schmitt, and Jennifer Slater, as well as
x • Acknowledgments

the anonymous reviewers who offered comments at an process, especially Clare and Iain and Morven, San-
early stage. dra who was so often a rock at work, Peter and Elisa-
Finally a thank-you to many colleagues and friends beth, and neighbor Pam; all of these have been
who have helped to keep me sane through this whole invaluable.
 Pa r t I

E s s e n t i a l s o f F l o we r
De s i g n a n d F u n c t i o n
This page intentionally left blank
 Chapter 1

W h y P o l l i n at i o n I s I n t e r e s t i n g

Outline ary trajectory of the plant. But the plant itself is im-
mobile, so that incoming pollen has to be borne on
1. Which Animals Visit Flowers? some motile carrier, sometimes wind or water but
2. Why Do Animals Visit Flowers? much more commonly on a visiting animal. To quote
3. How Do Flowers Encourage Animal Visitors? one source (Rothrock 1867), “among plants, the nup-
4. What Makes a Visitor into a Good Pollinator? tials cannot be celebrated without the intervention of
5. Costs, Benefits, and Conflicts in Animal a third party to act as a marriage priest”! A pictorial
Pollination overview of the stages is shown in figure 1.1, covering
6. Why Is Pollination Worth Studying? the processes of pollination that are the focus of this
book.
A flower also serves to protect the pollen as it ger-
minates and as the male nucleus locates the egg and
then to protect the ovules as they are fertilized and be-
The flowering plants (angiosperms) account for about gin their development into mature seeds. However,
one in six of all described species on earth and provide these later events (germination of the pollen and fer-
the most obvious visual feature of life on this planet. tilization of the ovule) are technically not part of pol-
In the terrestrial environment, their interactions with lination, and they are covered here only as needed to
other living organisms are dominant factors in com- understand the characteristics and effects of pollen
munity structure and function; they underpin all nutri- transfer.
ent and energy cycles by providing food for a vast Since flowers bring about and control plant repro-
range of animal herbivores, and the majority of them duction, they are central to much of what goes on in
use animal pollinators to achieve reproduction. Most the terrestrial world, and pollination is a key mutual-
of the routine “work” of a plant is carried out by roots ism between two kingdoms of organisms, perhaps the
and leaves, but it is the flowers that take on the crucial most basic type of exchange of sex for food; the plant
role of reproduction. gains reproductive success, and the animal—usually—
A flower is usually hermaphrodite, with both male gains a food reward as it visits the plant. But the visitor
and female roles. Hence it is essentially a structure does not “want” to be a good pollinator and has to be
that produces and dispenses the male gametophytes manipulated by the plant to move on and to carry pol-
(pollen), organizes the receipt of incoming pollen len to another plant. In practice, only about 1% of all
from another plant onto its own receptive surfaces on pollen successfully reaches a stigma (Harder 2000).
the stigma, and then appropriately guides the pollen’s Nevertheless, pollination by animals (biotic polli-
genetic material to the female ovules. The flower also nation) is both more common (Renner 1998) and usu-
protects the delicate male and female tissues (stamens ally more effective than alternative modes of abiotic
and pistils) and has a role in controlling the balance pollen movements using wind or water, and animal
between inbreeding and outbreeding, hence influenc- pollination is usually also associated with more rapid
ing the genetic structure and ultimately the evolution- speciation of plants (Dodd et al. 1999; K. Kay et al.
4 • Chapter 1

pollen grain

pollen

anther

pollen
stigma grain
stigma

pollen
conducting grains
tissue
style
anther Figure 1.1 The central processes of pollination in a
pollen typical angiosperm flower, with the route taken by
tube pollen from anther to stigma (followed by pollen tube
filament
growth into the style) in an animal-pollinated species.
ovary (Modified from Barth 1985.)

2006). Discussion of animal pollination therefore rably reveals the actions, both historical and contem-
dominates this book, and around 90% of all flowering porary, of the selective agents (mainly, but not solely,
plants are animal pollinated (Linder 1998; Renner the pollinators) that we know have shaped them. These
1998). Furthermore, plants are, of course, the founda- factors make floral biology an ideal resource for un-
tion of all food chains on the planet, and their efficient derstanding biological adaptation at all levels, in con-
pollination by animals to generate further generations trast with many other systems, where there are multi-
is vital to ensure food supplies for animals. Natural ple and often uncertain selective agents.
ecosystems therefore depend on pollinator diversity to In this first chapter, some of these central themes
maintain overall biodiversity. That dependence natu- are introduced to set the scene for more specialist
rally extends to humans and their agricultural systems chapters; it should be apparent from the outset that
too; about one-third of all the food we eat relies di- while each chapter might stand alone for some pur-
rectly on animal pollination of our food crops (and the poses, it cannot be taken in isolation from this whole
carnivorous proportion of our diet has some further in- picture.
direct dependence on animal pollination of forage
crops). Pollination and factors that contribute to the
maintenance of pollination services are vital compo- 1. Which Animals Visit Flowers?
nents to take into account in terms of the future health
of the planet and the food security and sustainability of At least 130,000 species of animal, and probably up to
the human populations it supports. 300,000, are regular flower visitors and potential pol-
Beyond its practical significance, the flower-animal linators (Buchmann and Nabhan 1996; Kearns et al.
mutualism has been a focus of attention for naturalists 1998). There are at least 25,000 species of bees in this
and ecologists for at least two hundred years and pro- total, all of them obligate flower visitors and often the
vides almost ideal arenas for understanding some of most important pollinators in a given habitat.
the fundamental aspects of biology, from evolution There are currently about 260,000 species of angio-
and ecology to behavior and reproduction. It is per- sperms (P. Soltis and Soltis 2004; former higher esti-
haps more amenable than any other area to providing mates were confounded by many duplicated namings),
insights into the balance and interaction of ecological and it has been traditional to link particular kinds of
and evolutionary effects (Mitchell et al. 2009). Flow- flowers to particular groups of pollinators. About 500
ers are complex structures, and their complexity admi- genera contain species that are bird pollinated, about
 Why Pollination Is Interesting • 5

250 genera contain bat-pollinated species, and about 3. How Do Flowers Encourage
875 genera predominantly use abiotic pollination; the Animal Visitors?
remainder contain mostly insect-pollinated species,
with a very small number of oddities using other kinds Many plant attributes contribute to attraction of visi-
of animals (Renner and Ricklefs 1995). tors: J. Thomson (1983) usefully groups these as plant
The patterns of animal flower visitors differ region- presentation. Some of these attributes are readily ap-
ally. In central Europe, flower visitors over a hundred parent to visitors, and these may be features of indi-
years ago were recorded as 47% hymenopterans vidual flowers (e.g., color, shape, scent, reward avail-
(mainly bees), 26% flies, 15% beetles, and 10% but- ability, or time of flowering) or features of whole plants
terflies and moths; only 2% were insects outside these or groups of plants (e.g., flower density, flower num-
four orders (Knuth 1898). But in tropical Central ber, flower height, or spatial pattern). The more readily
America, the frequencies would be very different, with apparent plant presentation traits can be divided into
bird and bat pollination entering the picture and fewer attractants (advertising signals), dealt with mainly in
fly visitors, while in high-latitude habitats the verte- chapters 5 and 6, which discuss visual and olfactory
brate pollinators are absent and flies tend to be more signals, and rewards (usually foodstuffs), dealt with in
dominant. Some of these patterns will be discussed in chapters 7–9. Aspects of the timing and spacing of
chapter 27. flowers, and how these might be affected by competi-
tion between different flowering plants, are given more
in-depth treatments in chapters 21 and 22.
2. Why Do Animals Visit Flowers? Other floral attributes are more cryptic to the visitor
and may only determine the reproductive success of
The majority of flower visitors go there simply for the plant in the longer term; these might include pollen
food, feeding on sugary nectar and sometimes also on amounts, ovule numbers, the genetic structure of the
the pollen itself. Chapters 7 and 8 will therefore deal in plant population, the presence and type of incompat-
detail with these commodities, and chapter 9 will cov- ibility system, etc.
er a few more unusual foodstuffs and rewards that can It is generally in the plant’s interest to support and
be gathered from flowers; chapter 10 will take an eco- even improve its visitors’ efficiency, encouraging them
nomic view of all these food-related interactions, in to go to more flowers of the same species (so ensuring
terms of costs and benefits to each participant. Major that only conspecific pollen is taken and received) and
themes in other chapters include the ways that flower to go to flowers with fresh pollen available and/or with
feeders can improve their efficiency: learning recogni- receptive stigmas for pollen to be deposited upon.
tion cues to select between flowers intra- and interspe- Many flowers therefore add signals of status to their
cifically, learning handling procedures, learning to repertoire, via color change, odor change, or even
avoid emptied flowers, and avoiding some of the haz- shape change. Visitors are thereby directed away from
ards of competing with other visitors. flowers that are too young or too old or already polli-
Flowers are also sometimes visited just as a conve- nated. Instead they will tend to concentrate their ef-
nient habitat, often simply because they offer an equa- forts on those (fewer) flowers per plant that are most in
ble sheltered microclimate for a small animal to rest need of visitation, thus also being encouraged to move
in, a place that is somewhat protected against bad around between separate plants more often and to en-
weather, predators, or parasitoids. Or flowers may of- sure outcrossing rather than selfing. Reasons for fa-
fer a reliable meeting site for mates or hosts or prey, or voring breeding by outcrossing (i.e., with other plants)
for females an oviposition site providing shelter for are covered more fully in chapter 3.
eggs and larvae. More rarely they are used as a warm-
ing-up site by insects in cold climates, usually because
the flowers trap some incoming solar radiation, which 4. What Makes a Visitor into
enhances their own ovule development, but occasion- a Good Pollinator?
ally because a few flowers can achieve some metabolic
thermogenesis that warms their own tissues (chapter 9 In many ways this is the crucial theme running through
will provide more details on this topic). this book. It relates to what is probably the major
6 • Chapter 1

current debate in pollination ecology, that is, to what Physical Factors

extent pollination it is a generalist process and to what
extent it is a specialist one. Pollination has in the past Any animal that is to be an effective pollinator must
nearly always been categorized in terms of syndromes, have the ability to passively pick up pollen as its body
with particular groups of flowers recognized as hav- moves past the anthers of a flower that it visits and
ing particular sets of characteristics (of color and carry that pollen to another flower. Normally this will
scent, shape, timing, reward, etc.) that suit them to be be aided by the animal being a good physical fit in
visited by particular kinds of animals; and it is im- terms of size and shape, so that in alighting on the
plicit in this approach that these suites have often been flower surface, or when inserting its tongue or beak of
arrived at and selected for by convergent evolution in appropriate length, some specific part of its body
plant families that are unrelated. Thus most authors touches the anther. Additionally pollen pickup and car-
have used terms such as ornithophily to describe the riage will be aided if the animal has appropriate sur-
bird pollination syndrome, or psychophily for the face structures; pollen adheres well to feathers, fur,
butterfly pollination syndrome. Flower characteristics and hairy or scaly surfaces in insects but does not get
would be listed that fit each syndrome, and an unfa- transported well on shiny or waxy surfaces (and may
miliar flower’s probable pollinators could therefore be even be damaged by certain surface secretions). Hence
predicted. Flowers in each category were seen as hav- a small shiny beetle taking some nectar by crawling
ing a degree of specialization that suited them to their into the lower surface of a large tubular corolla where
particular visitors, with some syndromes being more the anthers are in the corolla roof may well be a regu-
specialized than others. Nearly all earlier works on lar visitor to that flower but is unlikely to be an effec-
pollination were organized around this theme of syn- tive mover of its pollen; in effect, it is acting as a
dromes, and it served as a useful structure for under- “cheat” as far as the flower is concerned and may be
standing animal-flower interactions for nearly two termed an illegitimate visitor.
centuries. Without knowing this background it would
be nearly impossible to follow the current debates that
are a major focus for pollination ecologists, and it Behavioral Factors
would also be very difficult to structure the informa-
tion on flower attractants and flower rewards in chap- Different animals land on and forage at flowers in very
ters 5–9. This book thus retains a syndrome-based ap- different fashions. There are many aspects of behavior
proach throughout its early chapters and explicitly that will affect whether a given animal is going to be a
considers the evidence in support of a syndrome ap- good pollinator. Pollinators will seldom have a com-
proach in chapter 11; then it unashamedly covers each plete perception of all the aspects of plant presentation
of the syndromes in turn in chapters 12–19, providing mentioned above, but they will respond to at least
all the core materials on which later criticisms might some of them in ways that are useful to the plant:
be based.
The criticisms and debates focus around the reality 1. Their choices of places and times to visit, and ex-
of syndromes and how far they have been overplayed actly which flowers to visit, will be critical. Visits
in the previous literature, perhaps blinkering or bias- occurring before dehiscence (the splitting of the
ing our perceptions. Many authors now regard flower anthers to reveal the pollen) or after pollen deple-
pollination as a much more generalized phenomenon, tion are normally of no value to the flower in ful-
where most flowers get many different kinds of visi- filling its male role, and visits before or after the
tors and have not been and are not being heavily se- stigma is receptive to incoming pollen are of no
lected to specialize for the needs of one particular value to the flower in its female role.
“best” visitor. This approach is specifically addressed 2. Their handling of the flowers affect their pollen
in chapter 20. It will be a major argument there that the pickup and deposition characteristics; ideally they
issue has been clouded by an as yet insufficient dis- should receive pollen at a specific site on their
tinction between flower visitors and pollinators. So bodies, and one that is also a good site for subse-
what does make a visitor into a good pollinator? quent deposition of that pollen onto a stigma.
 Why Pollination Is Interesting • 7

3. Their handling time per flower affects how many late their body temperature and water balance more
flowers are visited in a given time. precisely; they generate heat internally through their
4. Their speed and directionality of movement be- own metabolism (endothermy) and regulate their own
tween plants affect pollen dispersal. body fluids with efficient skin exchanges, respiratory
5. They should not be too efficient at grooming off controls, and excretory organs. They can in principle
the pollen, or indeed at eating it. forage at almost any time and in any habitat, though
6. Their flower constancy, that is, the likelihood that they may still conserve their own energy by picking
they will move to another flower of the same spe- more equable sites.
cies, is perhaps most critical. If they innately or by The distinction does not lie exactly between the
learning prefer a particular flower phenotype, vulnerable invertebrates and the highly regulated birds
their high constancy will usually ensure that they and mammals, however. It is now clear that a rather
move neatly and sequentially among conspecific small proportion of insects can also show endothermy,
flowers, not wasting pollen by depositing it in the at least some of the time when they need to warm up in
wrong species. Constancy to a flower (considered the absence of solar inputs (chapter 10); this applies
in detail in chapter 11) gives economies to the vis- especially to most bees, a few hoverflies, some large
itor also; it may minimize travel distances, han- moths, and some beetles, occurring more sporadically
dling times, and learning effort and maximize pol- in other groups. It is perhaps no coincidence that endo-
len packing. thermic abilities in insects are most common in the
flower-visiting groups, which have access to ready
Behavioral factors such as these are often the key to
fuel supplies in the form of nectar but which may also
being a good pollinator and of course are affected by
need to compete for that nectar in the cool of early
the animals’ abilities to learn as they become more ex-
mornings or at dusk.
perienced as foragers. The ability to form a search im-
age or to respond consistently to other cues, associat-
Given the list of factors that can turn a visitor into a
ing particular signals with the presence of food, hones
good pollinator, two obvious points should emerge:
their foraging ability and can cement their relation-
ships with particular flowers. Hence later chapters of
1. A great many of the animals that go to flowers for
this book, in considering particular groups of animals
a short drink of nectar may be rather poor at pollinat-
that visit flowers, include careful consideration of their
ing that flower. Those with a poor physical fit, those
sensory and learning capacities.
that cheat, and those with little or no flower constancy
are likely to be especially ineffective.
Physiological Factors
2. Of all the visitors, bees are likely to be especially
Animals have differing physiological strategies and good as pollinators. They rely solely on flowers for
constraints, and these too can affect their energetic food, both as adults and as larvae, and so must visit
needs and thence their flower-visiting patterns, as will more flowers than any other animals. Their sizes, hairy
be discussed in chapter 10. Most animals (including surfaces, and variably long tongues, their excellent
nearly all invertebrates, and therefore many of the in- learning abilities, communication systems and floral
sect flower visitors) lack elaborate internal physiologi- constancy, and their endothermic capacities all equip
cal regulatory systems, and their thermal balance and them to visit flowers efficiently (from their own per-
water balance are strongly influenced by environmen- spective) and effectively (from the plant’s point of
tal conditions. They cannot function if they are too hot view). Although they are sometimes described as pol-
or too cold or are short of water, and must forage in len wasters (because they, or rather their offspring
times and places that provide suitable microclimates, back at the nest, eat so much of the pollen that they
using the sun’s radiation to warm up by basking, or pick up), they are by far the most important pollinators
shady places to cool down again, and seeking (usually) in most ecosystems, and they do achieve high pollen
sites that are relatively humid. However, birds and bats export from visited flowers (Harder and Wilson 1997);
are physiologically more sophisticated and can regu- plants have adapted over evolutionary time to make
8 • Chapter 1

best use of them by providing more than enough pol- offset the additional costs of animal exploiters: those
len to cater for their needs and ensure that sufficient visitors who take rewards without pollinating (thereby
pollen still commonly reaches other flowers. cheating, chapter 24) and the flower eaters (florivores)
or foliage herbivores also attracted by the pollination
cues (chapters 25 and 26). For the animals, there may
5. Costs, Benefits, and Conflicts in be costs linked to carrying the pollen they have inad-
Animal Pollination vertently picked up (sometimes it is very unwieldy and
can interfere with their wings or legs or sense organs),
Plants with hermaphrodite flowers benefit greatly be- which may favor animals trying to cheat, and there
cause a single animal visit can allow both pickup of may be costs also from the potential risks of predation
pollen and its deposition on a stigma, fulfilling both or parasitism at flowers, since enemies can use them as
the male and female functions of that flower at the a place to find prey or hosts reliably (chapter 24).
same time. Animals benefit greatly by finding easily There are also costs arising from the tendencies of the
acquired foods, both sugary (nectar) and often also plants to cheat (chapter 23) by offering no real reward
proteinaceous (pollen). Pollination by animals may and sometimes by trapping the animal.
therefore be a mutualism, of benefit to both partici-
pants, but it is not altruistic; for the animals, pollina-
tion of the flowers they forage at is almost always just 6. Why Is Pollination Worth Studying?
an irrelevant by-product. In fact the plant and animal
have a conflict of interest, often with adaptation and Pollination ecology can provide almost unparalleled
counteradaptation going on from both sides through insights into evolution, ecology, animal learning, and
evolutionary time to try and get a bigger share of the foraging behavior (fig. 1.2). It is perhaps the best of all
benefits. So the situations that we see now are the end areas to see and understand some basic biological pro-
products of the long and sometimes quite duplicitous cesses and patterns; studies that deal exclusively with
associations of flowers with animals. pollination biology have often had major impacts on
The plant ideally wants a visitor that is cheap to general ecological and evolutionary theory.
feed, alighting only briefly, moving on rapidly to an- Pollination interactions often show us evolution by
other plant, and being faithful to its chosen plant spe- natural selection in action almost before our eyes and
cies; so ideally, the forager should be chronically un- provide some very clear-cut examples of adaptive ra-
derfed and continuously on the move. But (again diation and, perhaps, of plant speciation. They are
ideally) the animal would prefer to be as well fed and particularly useful for studying coadaptations (co-
lazy as possible, getting as much food as it can from evolution), because such interaction often involve rel-
one flower with minimum energy expenditure, being atively few organisms interacting with relatively high
relatively sedentary, and then moving on to any other interdependence and incorporating the most funda-
nearby flower with copious nectar, whatever its spe- mental of phenomena (reproduction for the plant, food
cies (although we already noted that some degree of supply for the animal). There are selection pressures
fidelity may improve its foraging efficiency). on each side of the partnership, offering hopes that ef-
Hence, although there are obvious benefits to both fects at the basic level of male and female gene flow
partners, there are potentially clear costs as well. The can be quantified, sometimes (in crop pollination espe-
plant has to invest in attractants (its carbon and nitro- cially) on a time scale that can be detected within one
gen resources are used to make flamboyant petals, pig- scientist’s period of study.
ments, and chemical scents), as well as mere rewards. In terms of ecology, the study of pollination sheds
If the plant reduces its rewards too far, the animal may light on how different organisms interact and affect
not get enough food and will give up on that species. each other, especially the competitive effects of plants
The plant generally also has to compete with other upon each other, and on the various levels of interac-
plant species for pollination, to obtain a share of the tions of plants with pollinators, including resource al-
“good” pollinators, so it cannot afford to skimp on its location, competition, exploitation, and simply cheat-
offerings too much if it is growing within a reasonably ing. In the last two decades there has been an increasing
diverse plant community. Many plants also have to stress on community-level interactions in pollination
 Why Pollination Is Interesting • 9

Environmental factors

Energy balance/ Animal

economics Physiology

Ecology
Thermal Water Sensory
balance needs systems
FLOWER

POLLINATOR POLLINATION

Plant
Biochemistry
Rewards
Nectar Behavior
Pollen Evolution
Selection
Foraging
Learning Genetics
Searching
Advertisements Choosing Memory ST/LT
Colors
Handling Constancy
Odors
Shape/size Optimising

Figure 1.2 Key interactions of major biological topics and themes promoting interest in the study of pollination.

biology, now seen as an especially useful (because ment offering different proportions of alternative prey
highly quantifiable) arena for more general work on as potential food items of differing value (also taking
community structures (J. Thomson 1983); so this book into account factors such as conspicuousness and dif-
inevitably considers the community ecology of polli- ferent variances). The theory predicts that a range of
nation, especially in later chapters. outcomes from complete specialization on one kind of
Pollination biology also gives exceptional insight prey item to complete generalization on all possible
into the ecology of reproductive strategies and the items is to be expected, even from the same animal, as
complexities of sex and reproduction. Flowers usually the prey parameters are varied. Substituting “flower”
are hermaphrodites, but they have many ways of orga- for “prey item” (and with the immense advantage of
nizing their sex life sequentially or spatially to maxi- very easily quantified caloric rewards from nectar), it
mize their reproductive output and fitness. This book is not unexpected that pollinators similarly turn out to
contains rather little coverage of plant reproductive show almost the full range of possible foraging behav-
strategies beyond the basics, because the field has now iors. Furthermore, they have proved ideal subjects with
become dominated by theory and modeling, and the which to develop foraging models that can take into
topic has also been extensively and recently reviewed account different constraints on the foraging animals,
in other works (e.g., Harder and Barrett 2006). whether from different physiological limits or from
In the realm of animal behavior some key influ- different cognitive skills. Learning ability is especially
ences can be especially easily measured and manipu- needed where resources are of intermediate predict-
lated with flower visitors, and it is no accident that ability (Stephens 1993): that is, too unpredictable over
much of the key work on visual discrimination, learn- one or a few generations for fixed behavior patterns to
ing behaviors, and above all optimal foraging has be favored, but not so greatly unpredictable that an in-
used pollinators, especially bees. Optimal diet theory dividual cannot track the changes. This exactly applies
can model how animals should behave in an environ- to floral resources, so that we should expect flower
10 • Chapter 1

visitors from any taxon to be good learners. Fortunate- the models are sometimes hampered by reliance on in-
ly this is also readily tested with real or model flowers adequate records, and understanding, of flower-visitor
where just one trait at a time can be varied or associa- behaviors, and one of the most important issues for the
tions of traits compared; again, social bees are ideal immediate future is ensuring that the new generation of
animals to work with, reliably emerging from their pollination ecologists understand the core subject ma-
nests and traveling straight to the flowers provided, terial of floral biology and can measure and categorize
then displaying clear choices between alternative pollination as distinct from mere visitation to feed into
flowers. their models. We are in need of many and better quan-
titative studies of the effectiveness of visitors (for ex-
For all these reasons, and with the added concern over ample, the average number of conspecific outcrossing
human-induced effects on pollinator services in rela- pollen grains deposited on a stigma at an appropriate
tion to biodiversity and to crops, interest in pollination time by a given visitor in a single visit; chapter 11).
ecology has burgeoned in the last ten to fifteen years, Then we can properly understand plant and pollinator
and the subject is attracting strong interest beyond the communities and pollination networks, and the effects
traditional academic centers of the developed world, of potential extinctions of flower visitors/pollinators on
giving us valuable insights into more varied habitats in the communities of which they are a part. This book
Asia, Africa, and South America and into a greater di- therefore hopes to provide in a single source a useful
versity of interactions. Increasingly these systems are reference for all the aspects of floral biology and polli-
being modeled, and our preconceptions (of these and of nation interactions that need to be considered to give a
other kinds of mutualisms) are being challenged. But real appreciation of these fascinating mutualisms.
 Chapter 2

F l o r a l De s i g n a n d F u n c t i o n

Outline new supply (whereas animals normally are not modu-

lar and have a very limited and nonrenewable supply
1. Essential Flower Morphology of gonads). Investment in flower protection is there-
2. The Perianth fore often quite limited, but it may become paramount
3. The Androecium: Male Structures for species with only intermittent flowering, or with
4. The Gynoecium: Female Structures just a few large and expensively constructed flowers,
5. Flower and Inflorescence Features or with an extremely limited supply of pollinators; the
6. Particular Floral Shapes various ways in which flowers can be protected are
7. Flower Size and Size Range considered in more detail in chapter 24. Here we will
8. Flower Sex and Flower Design concentrate primarily on the design features related to
9. Overview: Essentials of Floral Design in sexual function in pollination.
Relation to Cross-Pollination Flowers come in an astonishing variety, whether
viewed across the entire spectrum of angiosperm fami-
lies (appendix) or merely one family at a time. A fam-
ily such as the Ranunculaceae has flowers ranging
from simple bowls (e.g., Ranunculus species such as
Flowers are essentially the containers for a plant’s sex buttercups) to complex bilateral pendant tubular de-
organs, but they must perform several interrelated signs with elaborate internal nectaries accessible only
functions. Most obviously, and taking center stage to long-tongued bees (e.g., many Aconitum) and to
here, they make and mature the gametes and then dis- tiny fluffy flowers where only the anthers are conspic-
pense the male gametes in such a way that they will be uous (e.g., Thalictrum). Other families show similar
transported to another appropriate flower in the pro- variation but often produce the same three broad kinds
cess of pollination, leading to fusion with female gam- of flowers, suggestive of convergent evolution.
etes. However, the flower must also be structured so Not only are individual flowers exceptionally var-
that it protects the crucial sex organs through pollina- ied in shape, size, and appearance, but the story is fur-
tion and seed set, both from the environment (exces- ther complicated by the tendency of flowers in many
sive rain or drought, freezing, heat load in full sun or families to mass together as inflorescences. Here the
during flash fires, physical damage in high winds) and overall floral display is determined by the combined
from herbivorous animals (whether these be tiny suck- appearance of a cluster of small flowers (sometimes
ing insects or large browsing and trampling verte- then termed florets) into one seemingly whole struc-
brates). The relative importance of the protective func- ture, which may in practice be the unit that is per-
tion in flowers varies enormously, and for many plants ceived, both by humans and by flower visitors, as the
the issue of protection of the living tissues is perhaps functional flower. We tend to refer to the complex mul-
less crucial than for most animals; plants are usually tiple inflorescence of hydrangeas, or of many umbel-
modular, with many sex organs in many flowers, so lifers, as their flowers; and we almost always speak of
that they can afford to lose some flowers and regrow a the floral displays in the composites (Asteraceae—
12 • Chapter 2

Table 2.1
Basic Floral Anatomy

Base Flower stalk or pedicel

Upward
and Inward Receptacle
Sepals Calyx
Perianth
Petals Corolla
Flower
Stamens Androecium
Carpels Gynoecium
Tip and center

daisies, asters, chrysanthemums, and their kin) as flow- flected in the inner series of stamens and carpels: in
ers, whereas in fact each is made up of many different the geranium family all the parts are in fives, and in the
florets, one kind making up the central disk and another lily and iris families all are in threes, but in some other
kind forming the outer rays, which appear as petals. families this numerical consistency is lost, often with
To consider flower design, then, we need to under- fewer carpels and more stamens than there are petals
stand both the key components of an individual flower, and sepals.
to analyze their juxtaposition within one flower, and to During flower development each part or series
review how the separate flowers can be assembled to- forms in sequence, and is in turn influenced by the ini-
gether, in many flower families, into complicated in- tiation and growth of neighboring structures. The orig-
florescences that become functional units in terms of inal apical meristem that will form the flower is pro-
display and attraction. tected in a bract, within which floral organs are
initiated; then as floral morphogenesis progresses, the
first series of structures, the sepals, grows and sur-
1. Essential Flower Morphology rounds the bud, within which the petals and the an-
droecium (male) and gynoecium (female) form se-
Flowers are complicated assemblages of plant parts, quentially. To add further variety, the fundamental
modified originally from leaves. Repetitive patterns of structures may fuse into a ring as they arise or during
units occur in series, growing centripetally and sitting ontogeny to form tubular organs. And sometimes parts
upon the flower stalk. Table 2.1 shows the general pat- of different floral organs may fuse, to form organ com-
terns of floral parts, with the four main series of struc- plexes. However, the basic underlying anatomy can
tures from base to tip, or outer to inner: sepals, petals, still usually be described by a simple floral diagram as
stamens, carpels. This fundamental structure can be in figure 2.1B.
detected in most flowers from the basic arrangement in The primary functions of flowers are always per-
figure 2.1A, though the details vary enormously; these formed by these basic and genuinely floral structures,
details can often be conveniently expressed in terms of but as we will see, some of the secondary functions
a simple flower diagram of the type shown in figure (protecting, guiding, advertising, and rewarding) may
2.1B. In particular, the numbers of each part are highly be taken over by organs outside the flowers.
varied: primitive magnoliids have very large numbers
of petals, as do cacti, but in many dicot plants there are
just five petals and five sepals, whereas in most mono- 2. The Perianth
cots these structures come in threes. Even here many
exceptions occur, and some important groups, such as The outermost structures of a flower collectively form
the crucifers (Brassicaceae) and the poppies (Papaver- the perianth; this sits upon the receptacle, which is
aceae), have their parts in multiples of two or four. really just the expanded often cone-shaped end of the
These petal and sepal numbers may or may not be re- flower stalk, or pedicel. The perianth itself may be
 Floral Design and Function • 13

Gynoecium pistil
Corolla
petal
stigma
A

style pollen
growing
pollen tube Androecium
embryo sac
nuclei ovules stamen
ovary sepal

Calyx receptacle

filament
anther
locule

Figure 2.1 (A) The basic structure of a flower, with both female (gynoecium) sepal
and male (androecium) reproductive parts (modified from Faegri and van der
Pijl 1979 and later sources). (B) A classical flower diagram showing an idealized B petal
structure in transverse section and the relation of the four major whorls of floral
parts.

protected by extrafloral bracts, which in some cases anthers

are brightly colored and serve both protective and ad-
vertising functions.
The perianth is made up of rather thin and flat struc-
tures that enclose and usually protect the rest of the nectary
flower, and its tissues are sterile (nonreproductive). At
anthesis (floral opening) the perianth commonly be-
comes a major part of the floral display, attracting the
pollinators. gynoecium with
There may be either one or two series of perianth carpels and ovules
parts. Where there is only one series (or occasionally
two but with no structural differentiation), the compo-
nent parts are usually called tepals. However, in the
majority of plants there are two series of distinctly dif-
ferent structures—the sepals and petals—forming the which the rest of the flower sits), either by sepals over-
perianth (as shown in table 2.1). lapping each other or by their fusion (producing the
condition called gamosepaly). Sepals can be formed
from a thickened epidermis that is relatively solid and
Calyx and Sepals free of airspaces or can be toughened by sclerenchy-
ma to give a semiwoody protective base to the flower;
The outer series of floral parts is mainly protective at in extreme cases, such as Costus, the sepals form a
all times in most plants and is termed the calyx, made lignified coating over the whole inflorescence through
up of sepals, often the same green color as the foliage which small cohorts of individual corollas emerge
but rather more robust. The calyx makes a cup (in (plate 34F, G). The external surface of a calyx may be
14 • Chapter 2

further protected with glandular hairs (for example, in viscous or mucilaginous material; for example, indi-
many Solanaceae) or with a waxy layer (for example, vidual Commelina (Commelinaceae) flowers (plate
in eucalypts). Either of these additions may help to de- 12A) emerge through a copious layer of thick muci-
ter possible folivores, and some of the waxy calyces lage held in the calyx, although the function of this
may also serve to reflect solar radiation, keeping the substance is rather uncertain.
base of the corolla relatively cool. Finally, there are cases of rewards deriving from
There are also quite a number of plant genera in sepals; by far the commonest examples are extrafloral
which the calyx sepals take on all or part of the role of nectaries, where glandular areas of the sepals produce
advertisement and pollinator attraction, both visual nectar that is predominantly collected by ants, in rela-
and olfactory (with scents from the glandular hairs). tion to their plant-guarding activities (chapter 25).
Sometimes the sepals form the main ring of colored Other examples are rare, although food bodies arising
visual attractants (and tend to be referred to incorrectly from sepals and fed on by beetles are not uncommon
as the petals); this is common in the Ranunculaceae, in the Winteraceae and in some Annonaceae.
including Helleborus (where petals may become nec-
taries; chapter 8), and many Anemone and Pulsatilla
species. Corolla and Petals
Alternatively just one or a few of the sepals are en-
larged and highly colored, giving the main visual sig- The inner series of the perianth structures is the co-
nal in some Rubiaceae and Verbenaceae. Something rolla, which is made up of petals and takes on the fa-
similar occurs in many euphorbs, such as Dalecham- miliar main display/advertisement function in most
pia (plate 11F), although there it is bracts rather than angiosperms. The petals tend to be arranged alternate-
sepals that produce the show (the “flowers” are in fact ly with the sepals (fig. 2.1B and examples in fig. 2.15).
compound inflorescences contained within the bright- As with sepals, the petals may be fused for all or part
ly colored bracts as a group of one female and several of their length (gamopetaly) to produce a tubular co-
male tiny flowers). Or attractive sepals may act in con- rolla. The color(s), size, shape, position, or orientation
cert with petals, whether being of the same color (e.g., of petals may all contribute to the attractiveness of the
the Salvia in plate 13G) or contrasting, as in some display.
Abutilon (plate 14A) and some Clerodendrum, or en- The petals are usually colored differently from the
larged, highly modified, and very differently colored foliage and are often more delicate in texture, with a
(plate 13F). In yet other cases, the use of sepals as ad- thin epidermis and a mesodermal layer that has plenti-
vertising structures occurs in only some flowers of a ful air spaces. However, thickened or fleshy petals are
complex inflorescence; the central flowers are of usual not uncommon, and thick, white or cream-colored co-
type, whereas outer ones have one or more enlarged rollas are often found in heavily scented dusk- or
colored sepals, increasing the showiness of the whole night-flowering species that are visited by bats or
floral display. Many Hydrangea species and hybrids moths using fragrance as an important cue. Petals may
are familiar temperate examples (plate 11E), as is co- release scent through their surfaces or bear specific
riander (plate 11D). scent-producing trichomes, or papillae (chapter 6). In
A further specialization occurs with the production some cases, particularly among the Magnoliaceae and
of a protective fluid by internal sepal surfaces, produc- Liliaceae, they bear nectar-producing tissues, and oc-
ing a water calyx, or water jacket (also achievable by casionally they provide a surface for secondary pollen
a cup-like calyx or leaf morphology that traps rainwa- presentation (chapter 7).
ter, as in many bromeliads). This moat of water around Petals may also present complex microtextured sur-
the flower base (plate 34D) may help to exclude ants faces, which provide easier landing platforms for
and other small visitors with little role in pollination visitors and may also play a role in close-up flower
(e.g., Carlson and Harms 2007; and chapter 24) and recognition (Kevan and Lane 1985). Textures involve
may also have a cooling function. Such watery calyces ridges, overlapping plates, or patterns of pimples, often
are well known in various tropical plants, including differing between the upper and lower petal surfaces,
many Bignoniaceae (they were first described in or between the upper petals and the lower landing-
Spathodea from this family). Other genera produce platform petals in bilateral flowers. For example,
 Floral Design and Function • 15

through direct tactile perception, bumblebees could lengths of up to 50 mm. This length is often achieved
discriminate among flowers of Antirrhinum mutants quite late in the floral development process, and elon-
that lacked special conical epidermal cells on petal gation can be very fast; in some grasses the filament
surfaces (Whitney, Chittka, et al. 2009). can grow several millimeters in just a few minutes as
Occasionally the petal tissues, or parts of them, dehiscence approaches. On average, filaments are
combine with parts of the next inner ring of tissues somewhat longer in grasses and other anemophilous
(the stamens) to form a corona. This appears as an “in- (wind-pollinated) flowers than in zoophilous (animal-
ner corolla” in flowers such as daffodils, where it pollinated) species. However in many of the zoo-
forms the protruding trumpet (plate 6E), and in pas- philous flowers with fused petals, the filaments are
sionflowers (plates 5A,B and 26G), where the corona inserted onto the inside of the resulting corolla tube
is filamentous and becomes an elaborate inner circle of (adnate filaments; e.g., fig. 2.2F–H) rather than arising
contrasting display. basally, so they are technically short but still function
Both series of perianth structures are usually wilted as if they were elongate. Rarely, the filament is elabo-
or shed after anthesis, and in some plants, pollination rated with fine hairs (easily seen in many Verbascum
per se, or the fertilization of the ovules that follows species) or with nodular thickenings (e.g., in Spar-
pollination, may act as a trigger for the wilting or se- mannia), which may enhance their visual signaling ef-
nescence of the corolla. However, sepals are some- fect (fig. 2.2K).
times retained to assist in fruit development (for ex- The filament is usually attached to the base of the
ample becoming the wings of the nuts in the large anther, but sometimes anthers are suspended close to
Southeast Asian dipterocarps) or to provide a con- their midpoint by a thin and flexible junction; this is
trasting background for fruit advertisement. Petals seen in many Liliaceae (fig. 2.2J; plate 12C), where
may wilt on the calyx or may be shed by a specific the anthers hang down and move freely in seesaw
abscission mechanism involving ethylene (a common fashion about this joint.
within-plant signaling system). But even petals are oc- Within the anthers, the main design variation is in
casionally retained and thickened to form part of the the location and form of the furrows that split apart at
fruiting structure. dehiscence (fig. 2.3). Most commonly the furrows (or
thecal slits) open toward the center of the flower (in-
trorse anthers), so that pollen is presented inward in
3. The Androecium: Male Structures the direction of the female organs; in flowers visited
by larger animals, such as bats or birds, the introrse
The male functional organs of a flower, collectively anthers may open broadly to produce a flat pollen-
termed the androecium, are a series of stamens. Each dispensing surface that can press against fur or feath-
is formed from a thin filament, which may be erect, ers, as seen in many passionflowers (plate 5A,B). Ex-
curved or pendant and which supports the terminal an- ternally or laterally opening anthers (extrorse or
ther. The most common type of stamen has an anther latrorse, respectively) are also found, but less com-
with four pollen sacs (or locules), arranged in two monly; they tend to be smaller and are borne on shorter
pairs, each pair termed a theca. The thecae open at filaments. Occasionally, there is only one furrow and
maturity in the process termed dehiscence, so expos- the locules are united internally to open as a single
ing the pollen (dehiscence and its control will be cov- chamber; Pavonia is a good example. At the opposite
ered in chapter 7). extreme, the locules may subdivide internally (either
Relative to other flower parts, stamens are rather transversely or longitudinally) to give a polysporan-
constant in size and shape and design (see the review giate anther. Sometimes dehiscence slits may lose the
by Bernhardt 1996). In the phylogenetically basal fam- standard elongate pattern and become curved or al-
ily Magnoliaceae, the distinction between the anther most circular on the tip of a bulbous anther head, giv-
and the filament is poor, but in nearly all other flowers, ing a valvate stamen (fig. 2.2E).
a two-lobed anther sits on the end of a much thinner In some plant groups, especially zoophilous taxa,
and elongate filament. Stamens are rarely more than stamens are modified by becoming united into a more
20 mm long, although in some plants the filaments are complex structure (fig. 2.4), a phenomenon known as
fused basally and can then be strong enough to support synandry. This is quite common in the large orders
16 • Chapter 2

A B C D

E F G H

I J K L
Figure 2.2 Stamens with different filament and anther arrangements: (A–C) simple patterns with dehiscent slits on
anthers; (D) elongate with elaborate dehiscence furrow; (E) anther rounded and valvate; (F–H) adnate filaments aris-
ing from petals, internal or protruding, in various Boraginaceae and Caprifoliaceae; (I) dimorphic stamens set at two
heights in Oxalis; (J) seesaw anther head on filament, in Lilium; (K) filament with nodes in Sparmannia; (L) anther
with terminal pore in caesalpinoid Fabaceae. Not to scale.

Malvales and Fabales, and it may involve just the fila- or Cassia, giving a single pollen-dispensing structure
ments or the more distal anthers as well, resulting in a that a visiting bee can grasp and vibrate its body
tubular androecium (or even a solid cylindrical struc- against, and in these kinds of plants, it is commonly
ture if there are no female organs in that flower). This associated with loss of the anther’s dehiscence fur-
greater rigidity in the central floral organs may provide rows and their replacement with one or more terminal
a stronger area to grip or to maneuver around for in- or lateral pores through which pollen emerges (pori-
sect flower visitors. A further possibility is for the an- cidal anthers). Single-pored anthers are also found in
thers to unite at the tips but without the filaments doing other situations: in some bellows flowers, such as Cy-
so; this is often seen in composite flowers (see Com- phomandra, that are squeezed by a bee to release the
posite Flowers below). It also occurs in many buzz- pollen, and in some of the carrion flowers that attract
pollinated plants (chapters 7 and 18), such as Solanum flies, where the anther is polysporangiate internally
 Floral Design and Function • 17

factory signalling. Where they are long and protrud-

A ing, they markedly increase the apparent size of the
flower or inflorescence and may result in a brush blos-
som (see Brush Blossoms below). Where the rest of
the perianth is very small, the anthers then become the
main visual signal. While anthers are commonly brown
or dull in color when closed and take on the color of
the pollen when dehiscing (usually yellow; but see
chapter 7), the filaments are often white or almost col-
orless and so may provide a visual contrast to enhance
visibility of the pollen. In a few cases the filaments
change color very strikingly as a flower ages (or per-
haps as it is pollinated); one case is Koehneria from
Madagascar (plate 16E). Scented stamens are known
in some Chloranthaceae and Solanaceae (including
Solanum), again enhancing the flower’s attraction. Ad-
ditional functions include guidance for the tongues of
B C pollinating visitors, especially where the corolla is tu-
bular but quite wide, and exclusion of the tongues of
inappropriate/illegitimate visitors, by such features as
hairiness (sometimes as a band of hairs on the filament
at a particular depth) or by partial fusion, where the
stamens insert onto the sides of the corolla, as in many
composite flowers (see Composite Flowers).
The most obvious variation in androecium struc-
tures comes with heteranthy (also termed heteranth-
ery), the phenomenon of having two kinds of anther
(fig. 2.5). In its less dramatic forms, heteranthy in-
volves two whorls of stamens within a flower that are
slightly different in developmental rate and so appear
morphologically distinct almost until they dehisce; in
Figure 2.3 Anther heads: (A) transverse section showing internal
these cases there may be little or no functional differ-
structure; (B) transverse section of typical tetrasporangiate anther
with two locules, closed and then open at dehiscence; (C) longitudi-
ence between the two sets, although where the two
nal dehiscence (left) and valvate dehiscence (right) seen in frontal groups are set at different heights, they may exploit
view, x–x marking the dehiscence furrows. (Redrawn from Endress two different kinds of flower visitor. The more extreme
1994.) versions, seen in fig. 2.5 and in examples on plate 12,
occur where one set of anthers is relatively cryptic and
bears the reproductively important pollen, while the
but where aggregated pollen emerges from the single other is showier and contains fodder pollen (chapter 7).
pore in a slimy thread or droplet. One other specializa- Several genera in the Lecythidaceae have hundreds of
tion to be noted is the phenomenon of sensitivity in stamens per flower: in the cannonball tree Couroupita,
stamens: in a number of plant families the filament is there are prominent central feeding stamens, plus a
somewhat contractile and may shorten or curve in one semicircle of stout pollinating stamens set on an an-
direction when stimulated by a visitor (chapter 7 and droecial hood around the lower half of the flower, de-
Compsite Flowers below). positing pollen on the feeder’s undersurface. Even
As well as dispensing pollen, whether partly as a more extreme are some of the blue-flowered Commeli-
reward or solely for reproductive purposes, stamens na species (plate 12A), with three kinds of stamen and
may serve some other important roles. They are often anther: two cryptically blue and lateral, one central
used in advertisement and attraction, via visual or ol- and either blue or yellow, and three shorter and bright
18 • Chapter 2

T.S.
a a at a–a

b
B
b
T.S.
at b–b

Figure 2.4 Examples of synandry (full or partial fusion of anthers centrally) in various angiosperms: (A) Solanum;
(B) Dodecatheon (shooting star); (C) Sprengelia, transverse section showing basal separation and terminal fusion of
anthers. (Parts (A) and (B) redrawn from Buchmann 1983; part (C) drawn from flowers.)

yellow (usually termed staminodes; see below). All but are sterile and have no reproductive function. They
produce viable pollen, but that from the staminodes is may augment the visual display (Theobroma or Jaca-
much less viable; the lateral stamens achieve most of randa, fig. 2.5) or have scent-emitting tissue (osmo-
the cross-pollination, the central one provides rewards phores) or secrete some nectar, and in some cases they
to pollinators (and some delayed selfing possibilities), can move during the life of the flower, bending over to
and the yellow staminodes serve as bright attractive protect the female structures.
signals mimicking copious pollen on offer (Hrycan
and Davis 2005). Other species of Commelina have
rewarding yellow anthers, unrewarding yellow an- 4. The Gynoecium: Female Structures
thers, and brown reproductive anthers, and removal of
either of the first two types reduces pollen export from The female organ system, technically the gynoecium,
the third (Ushimaru et al. 2007). is the most central part of the angiosperm flower, and
The design and size of stamens may usually be while superficially rather simple, it is internally very
relatively constant, but variability in stamen number is complicated, having interconnecting chambers and ca-
extreme. Flowers may contain just one stamen, as in nals. The gynoecium is made up of one or several pis-
most asclepiads and most orchids, or may have several tils, each of which contains one or more carpels. Most
hundred, as in some Cistaceae and Myrtaceae. Occa- flowers have several carpels, two to five being the most
sionally there are in excess of two thousand stamens in common, though these may be laterally fused together
a flower. Indeed, almost this full range can occur with- more or less completely (syncarpy) and thus contrib-
in just one order of plants: Ascarina has one stamen ute to only one pistil (the advantage of this being that
and Tambourissa has about two thousand, both being received pollen can be distributed among all the car-
in the Magnoliidae. pels after successful pollination). Rarely the number
Staminodes are structures formed from the same of carpels is huge, up to about two thousand in Tam-
series of embryonic tissues as the functional stamens bourissa, which as noted above also has around two
 Floral Design and Function • 19

upper
fertile sterile
anthers stamens

gynoecium
style

lower fertile
lower fused stamens
sterile anthers
Couroupita Cassia

two enlarged
petals
style

fertile
anther

Two distinct
lengths of
Two stamens
feeding
anthers

Commelina Mouriri

one of five whole flower

staminodes one of four
normal anthers Close up of
style reproductive
style
structures

fertile
anthers petals
staminode
Theobroma Jacaranda

Figure 2.5 Heteranthy in various flowers, where stamens come in two different forms: different lengths, as in Mouriri,
or modified for feeding and reproductive purposes, as in Couroupita, Commelina, and Cassia; or with one or more
modified as staminodes in Theobroma and Jacaranda. (Couroupita and Commelina modified from Endress 1994;
Mouriri and Cassia modified from Buchmann 1983; Jacaranda and Theobroma drawn from photographs and
flowers.)
20 • Chapter 2

A B
a a

a b b
a

c
b

b c
c d d
c

Figure 2.6 Basic gynoecium and ovule structures

C D in medial long section and the associated termi-
nology. (A) Unicarpellate (i.e., gynoecium with a
single carpel containing two or more ovules);
(B) syncarpous, here with two carpels; (C) pat-
terns of curvature as the ovule develops: (from
left to right) orthotropous, anatropous, and
campylotropous; (D) ovule curvature relative to
carpel curvature, (left) syntropous and (right) an-
titropous. (Redrawn from Endress 1994.)

thousand stamens. Only in the legumes is a unicarpel- divisions of the embryo sac are shown in figure 2.7;
late state commonly found (though legumes are so the end result is eight nuclei, one of which at the mi-
numerous that this may amount to around 10% of all cropylar end of the ovule becomes the egg itself, which
angiosperms). after fertilization from a pollen grain will become the
Pistils and carpels can be rather complicated, and plant’s seed (chapter 3).
their terminology is confusing for nonbotanists. For The number of ovules in a flower is highly variable:
pollination biologists, the term “pistil” is the most use- many plants have only one ovule per carpel, a state
ful to remember, because unisexual flowers (or phases seen in grasses and most of the Ranunculaceae (in
of flowers) are often referred to as pistillate and sta- which case, the term “ovary” is redundant); but at the
minate to indicate female and male, respectively. In other extreme, orchids may have thousands of ovules
practice, for most pollination studies it is only neces- per carpel.
sary to consider two key zones of each pistil or carpel: The style is a rather diverse organ both in size and
the apical surface, which forms the stigma on the tip of in shape, with a more or less distinct stigmatic surface
the more or less elongate style, and the underlying at its tip (fig. 2.8). Larger styles are common in wind-
ovary, comprising one or several ovules (fig. 2.6). pollinated flowers and in those with many ovules.
Each ovule consists of an undifferentiated multicellu- Whatever the size, styles are sometimes of a compact
lar mass termed the nucellus, which is surrounded by and cone-like shape, but more commonly they are elon-
an integument that leaves open only a narrow apical gate with stigma and style distinct from each other.
channel, the micropyle. The basal end of the ovule is The style often forms a fairly rigid central column in
attached to the rest of the carpel via a short stalk. As the flower in insect-pollinated species, its main func-
the flower matures, one cell within the nucellus under- tion being to get the stigmatic surface into the “right”
goes meiosis to give four haploid cells, and one of position, but it may also be providing grip for some
these enlarges as the embryo sac. The normal further visitors and perhaps preventing too much damage
 Floral Design and Function • 21

pollen
three tube generative
antipodal nucleus
nuclei

embryo
sac tube
nucleus

female
polar nuclei egg sperm
nuclei
synergids

polar nuclei
endosperm and sperm

egg and
sperm

zygote

mass of
endosperm

embryo

Figure 2.7 Five stages in the divisions of the embryo sac during typical fertilization in an angiosperm.
22 • Chapter 2

Simple columnar or Bilobed styles

capitate styles

Elongate styles Divided styles

Malva Crocus Vinca Vulpia Iris

More complex or elaborate styles

Figure 2.8 Varieties of styles and stigmas in angiosperms, ranging from typical short columnar structures to elon-
gate and highly divided forms and including the crested styles of Crocus and the enlarged petaloid styles seen in
Iris. Not to scale. (Malva, Crocus, Vinca, Vulpia, Iris redrawn from Barth 1985; others redrawn from photographs and
flowers.)

during nectar-seeking behaviors. Quite commonly the 2006). In some flowers the style is strongly asymmet-
style elongates throughout the life of the flower, so that rical, bent to one side of the flower (plate 12F–H),
it starts shorter than the anthers and later grows to while in irises the style can become petaloid, and its
match or exceed them in length, thus facilitating for- partly tubular form helps to restrict and control polli-
eign pollen pickup (chapter 3). Occasionally the style nator access (plates 9C and 15C).
recurves as it grows, and this can be influenced by pol- Many stigmas have a somewhat lobed tip, with
len deposition to promote outcrossing while allowing three or five stigmatic lobes (plate 12G) being the
selfing as a backup or safety net (e.g., Yu and Huang most widespread patterns, reflecting the presence of
 Floral Design and Function • 23

three or five carpels in the major plant families. Bi- 2. Pollen recognition, then
lobed, forked styles are also common (plate 12F). The 3. Pollen adhesion and lectin binding, and finally
surfaces of the lobes are often strongly textured, with 4. Pollen germination, for which there are also zones
many papillae or with a feathery (plumose) appear- with enzyme-secreting activity, often particularly
ance: in some Crocus species the stigma has showy associated with high levels of peroxidase during
lobes and crests (plate 3G). This surface may also be peak receptivity.
described as wet (sticky) or dry. The wet/dry categori-
Pollen grains commonly imbibe water from the stigma
zation is probably not very helpful in relation to polli-
and germinate within a few hours of their initial depo-
nation; most stigmas have some form of stigmatic
sition. Germination does not happen in water alone,
exudate, usually lipid rich and markedly hydropho-
but for some species it can be induced in simple sugar
bic, so that an appearance of stickiness merely indi-
solutions, suggesting a fairly uncomplicated osmotic
cates how abundant this exudate is at a particular time.
effect. The pollen tube emerges into a mucilaginous
However this wet/dry distinction is often important in
secretion, which may provide some of the nutrients re-
relation to the mechanisms of self-incompatibility in
quired for later stages of pollen tube elongation.
the plant (covered in chapter 3): wet stigmas are rela-
Within the style is a pollen tube transmitting tract
tively free of protein material and are not selective for
leading down to the ovules. This tract may be epider-
pollen adhesion, whereas dry stigmas have thin pro-
mal or may involve deeper tissues, depending on the
teinaceous exudates and only the conspecific pollen is
taxon; in groups with very numerous ovules (especial-
retained.
ly the Orchidaceae, but also including some Ericaceae
Several other stigmatic phenomena are important
and Rafflesiaceae), the tract is particularly well devel-
for pollination, and most of these relate to temporal
oped and secretes substantial mucilage internally. Pol-
patterning. The timing of the secretion of the stigmatic
len tubes can cross between carpels readily in this
exudate may be important and is often carefully con-
tract, so that their final destination in terms of meeting
trolled, occurring in one or more waves; it may itself
an ovule is not predetermined by where they landed
be triggered by pollination. Likewise, the timing of the
on the stigma. However, as the tract approaches the
opening (or closing, or both) of the stigmatic lobes is
ovules, it splits into separate parts, one for each carpel
crucial in many flowers in relation to determining
or ovule. Growth in the tracts is normally unidirec-
when pollen can be received; in some flowers, the stig-
tional, from stigma to ovule, but if pollen is introduced
ma exhibits sensitivity and can close when touched. In
experimentally at a midpoint, it can often grow equally
bladderwort (Utricularia), the two stigmatic lobes rap-
well in either direction. The act of pollination may
idly fold together after being touched by a bee entering
cause the ovary to release a growth stimulus for pollen
the flower. In monkey flowers (Mimulus), physical
tube elongation, providing a pulsed gradient of chemi-
contact produces a faster closure than pollen arrival,
cal signals that the pollen tube follows down to the
and touched stigmas with no pollen will normally re-
ovules; ions and protons are implicated, and calcium/
open within 2–5 hours (Fetscher and Kohn 1999),
calmodulin signaling is also involved (Holdaway-
whereas pollen receipt produces delayed reopening or
Clarke and Hepler 2003; Shi et al. 2009). It also seems
permanent closure (fig. 2.9).
likely that the style tissues help to transport the pollen
The surface of the stigmatic lobes is primarily re-
tube, since tiny latex beads introduced into the style
sponsible for determining whether a pollen grain that
can be seen to move toward the ovules at a speed simi-
has landed there will germinate or not. This surface
lar to that of tube elongation (Sanders and Lord
has a limited period of receptivity to pollen, which
1992).
may vary from just a few minutes in some grasses to
Only rarely is this pollen tube tract absent in angio-
around 4 to 5 days in tomato (Lycopersicon, now in-
sperms. However, in a few self-fertilizing cleistoga-
cluded in Solanum) and up to 3 weeks in some orchids.
mous flowers (chapter 3) pollen can germinate within
The surface is structurally and chemically complex,
the anthers where it was produced and grow down the
with receptor sites concerned with several phases of
filament or through the anther wall to the stigma.
pollination and beyond:
The ovary of the flower is the most crucial organ in
1. Pollen hydration (which may take only a matter of reproductive terms, and its relationship to the recepta-
minutes), then cle on which the whole flower sits is important. In
24 • Chapter 2

stigmatic
lobes

pollinator B
visitation
ovary

Figure 2.9 Stigma behavior in Mimulus auran-

D tiacus, with initial closure in response to touch
or visitation, followed by (A) quick reopening
if there has been no pollen receipt, or (B)
somewhat delayed reopening with some pol-
len receipt, or (C) a slow reopening with more
Senescence pollen but few fertilized ovules, or (D) perma-
0 2.5–4.5 20–28 of flower
nent closure if fertilization levels are high.
Time (h) (Modified from Fetscher and Kohn 1999.)

many flowers the receptacle forms a simple (often where the receptacle can give some much-needed pro-
nectar-secreting) dish on which all the true floral parts tection against damage from a bird’s bill.
sit, with the carpels at the center; but in other cases the Arrival of a pollen tube within the ovary and close
receptacle has become deeper and sturdier, with the to an ovule may occur some hours after pollination,
carpels more or less embedded within it, and the other this interval depending in part on the length of the
floral structures then appear to be borne above the style. Pollen tube arrival initiates the series of events
ovary. Ovaries in the latter case are termed inferior that lead to fertilization and the successful reproduc-
(seemingly lying below the point of origin of the se- tion of the plant, which will be discussed in chapter 3.
pals, petals and stamens) as opposed to superior ova-
ries, where the outer floral structures clearly arise be-
low the base of the ovary (fig. 2.10). There are many 5. Flower and Inflorescence Features
possible intermediate states, but in some of the major
families this character is fairly fixed and is a useful aid Single Flowers and Inflorescences: Functional
to identification (table 2.2). Inferior ovaries are rare in Units and Blossoms
more phylogenetically basal plant families and are
generally assumed to be an evolutionarily more ad- Basic floral anatomy not only can yield the full range
vanced state resulting from selection for increasing of familiar single flowers but also allows flowers to be
protection by the receptacle. However, changes and arranged en masse to form a composite inflorescence
reversions in this ovarian position character are fairly with very different appearance and handling needs
common; for example, ecological considerations may (plates 1 and 11). The latter may be a loose open struc-
intervene, and bird-pollinated plants even from more ture, with individual flowers set well apart, or it may
basal taxa are often found to have inferior ovaries, form a compact mass, with flowers almost or actually
 Floral Design and Function • 25

1
A

C
2 D

Figure 2.10 Superior (1) and inferior (2) ovaries, resulting from different rates of expansion of the enclosing and ad-
jacent tissues. Meristem tissue is stippled in A and B. The thick line represents corresponding tissues in (B), (C), and
(D) to clarify relative expansions. (Redrawn from Endress 1994.)

touching. An inflorescence may be perceived as a sin- likely that dense packing of a flower head can be a use-
gle display unit—effectively as one large flower—by ful strategy for avoiding, or at least reducing, illegiti-
most visitors and is commonly referred to as “a flow- mate visits to flowers, preventing access by those visi-
er”; a single daisy or thistle or scabious is almost self- tors who might otherwise bite into the bases of the
evidently “one flower” in all practical senses. A useful corolla tubes and steal the nectar (chapter 23).
convention is the use of the term blossom for a func- The form and structure of inflorescences are sum-
tional unit. Thus a single buttercup or foxglove or or- marized in figure 2.11 and table 2.3. Although the ter-
chid is a blossom, a daisy or a willow catkin is a blos- minologies given there seem fairly clear-cut, in prac-
som, and at the opposite extreme, just one of the three tice many inflorescences defy easy classification and
parts of a single iris flower may serve functionally as a have mixed characters (e.g., many labiates are race-
blossom (see below). mose, but the branches within the raceme are dicha-
The various tight packing arrangements seen in the sial cymes). For practical purposes, it is usually easier
inflorescences (sometimes called “flower heads”) of just to refer to an inflorescence; botanical taxonomists
umbellifers and composites may have the benefit of need the more complicated approach, but pollination
producing a large landing platform for the many kinds biologists usually do not.
of visitor that cannot hover while feeding, while si- The differing structures of inflorescences can nev-
multaneously keeping individual flowers very small, ertheless have marked effects on visitor behaviors.
matching the size of the visitor’s mouthparts (rather Jordan and Harder (2006) compared bumblebee visits
than accommodating the visitor’s whole head or body, to racemes, panicles, and umbels each with 12 flowers
as is usually appropriate for a single flower). It is also and found that the bees visited slightly more flowers
26 • Chapter 2

Table 2.2
The Position of Ovaries within the Flowers of Some Major Plant Families

Always superior Always inferior Variable

Monocots Alliaceae Orchidaceae Agavaceae

Commelinaceae Iridaceae Araceae
Musaceae Bromeliaceae
Zingiberaceae

Dicots Acanthaceae Apiaceae Ericaceae

Apocynaceae Araliaceae Lythraceae
Boraginaceae Asteraceae Nymphaeaceae
Caryophyllaceae Caprifoliaceae Rosaceae
Cistaceae Cornaceae Saxifragaceae
Convolvulaceae Hydrangeaceae
Fabaceae Myrtaceae
Gentianaceae Onagraceae
Geraniaceae Rubiaceae
Magnoliaceae
Malvaceae Begoniaceae *
Papaveraceae Cactaceae *
Polemoniaceae
Scrophulariaceae
Solanaceae
Verbenaceae
Violaceae
Primulaceae *

* usually rather than always.

on the umbels but had far more consistent foraging Vallius (2000) explored this effect in the orchid Dac-
paths on the raceme, which (combined with different tylorhiza and found upper flowers to be smaller, to
temporal regimes of pollen presentation, discussed in have lighter pollinia, and to produce smaller seed cap-
chapter 3) should lead to less selfing on the racemes sules; but these effects could be ameliorated if lower
than on umbels. flowers were removed artificially, which suggests
Likewise, the position of flowers on inflorescences some influence from resource allocation. Kliber and
can markedly affect their characteristics, as shown in Eckert (2004) tested the underlying causes of this in
table 2.4 for a typical umbel (the carrot, Daucus; Aquilegia canadensis and found that detailed aspects
Perez-Banon et al. 2007). Here the lower orders of of floral morphology (nectar-spur length, sepal size)
umbel have fewer flowers each and a higher propor- showed very little sequential change. However, ovule
tion of male-only flowers, so that the overall sex of the and pollen production declined by 9% and 18%, re-
plant changes as it ages; so too does the sex ratio on spectively, with flower sequence up the spike, an
an individual umbel (fig. 2.12B), and thus the plant effect that could be modified in either direction by re-
as a whole has male phases alternating with female/ source availability. In this plant the main adaptive
hermaphrodite phases (fig. 2.12C). reason for sequential decline in allocation was proba-
There is often a sequential decline in resource al- bly herbivory, which was greater on the higher and
location among flowers on an inflorescence as well. later flowers.
 Floral Design and Function • 27

x x
x

Simple Compound Helicoid Simple Compound

Cymes Corymbs

Spike Scape Raceme Panicle

(= branched raceme)

x
x x
x
pedicel
umbellet
involucra ray
(cluster of bracts)

Head/Capitulum Simple Compound Verticil

Umbels

spadix spathe

flower cluster

Spadix with spathe Thyrse Catkin

Figure 2.11 The terminology for different types of inflorescence. (X indicates the oldest flowers in each case.)
28 • Chapter 2

Table 2.3
The Structures and Terminology of Inflorescences

Structure Term

Oldest flowers at base Racemose inflorescence

Flowers stalkless  Spike
Flowers stalked  Raceme
  Stalks all or mostly branched    Panicle
  Varied stalk length to give flat top   Corymb
Oldest flowers at apex Cymose inflorescence
 Two branches paired below apex  Dichasial cyme
 Single branch, to one side  Scorpioid cyme
All flowers radiating from common point Umbel
All flowers stalkless on top of stem Head or capitulum

Table 2.4
Variation in Characteristics on the Umbels of Daucus carota

Total flowers Hermaphrodite flowers*

Umbel position No. of umbels per umbel (%)

Central 1 4,829 61.0

Primary 17.6 4,895 33.6
Secondary 84.4 3,006 16.1
Tertiary 55.7 1,223 15.6

Source: Modified from Perez-Banon et al. 2007.

*Hermaphrodites are peripheral and males central.

Symmetry al. 1999; Glover 2007), and is organized via a floral

symmetry gene network that may be linked to plant
As shown in figure 2.13, there are essentially two main breeding systems (Kalisz et al. 2006). In modern
types of symmetry in flowers: radial symmetry (also plants, radial symmetry occurs in around 80% of all
termed actinomorphic, or regular) and bilateral sym- families, and bilateral symmetry in 33% of dicot fami-
metry (or zygomorphic, or dorsiventral, or lateral; lies and 45% of monocot families (Neal et al. 1998);
also sometimes termed irregular) (Endress 1999). the evolution to bilaterality probably occurred repeat-
Neal et al. (1998) gave a detailed review of the termi- edly by parallel recruitments of cycloidea homologs
nology and confusion that can arise, as summarized in (Preston and Hilernan 2009).
table 2.5. Radial symmetry is clearly the ancestral or Radial flower shape offers similarity of approach
primitive state, being present in the more ancient plant and landing from any direction, simplifying the pat-
families, and it remains very common; but bilaterality tern recognition task for the visitor. It is generally also
has evolved and been lost repeatedly (Ree and Dono- associated with a radial offering of rewards: either a
ghue 1999). This has happened at least partly because complete ring of nectary tissue around the base of the
the switch from radial to bilateral symmetry can occur ovary or a series of separate nectaries related to the
very easily, often involving just one or two genes (cy- number of petals present, plus a mass of central an-
cloidea, dichotoma) (Coen and Nugent 1994; Cubas et thers. A radial flower can therefore be accessed and
 Floral Design and Function • 29

C
A

L1
L2 L2
L1
L3
L3
L2
L2

B
1200
Hermaphrodite flowers
1000 Male flowers
Cumulative no. of flowers

800

600

400

200

0
0 2 4 6 8 10 12
Flowering days of an umbel
Figure 2.12 The sexuality of individual flowers
in relation to flower position within an umbel:
(A) the orders of flowers—C, central; L1, pri-
mary lateral; L2, secondary lateral; L3, tertiary
C
lateral; (B) peripheral flowers are hermaphro- male female
dite and open first, with central male flowers
opening later, and each successive order of
lateral umbels produces the same sequence,
C L1 L2 L3
leading to an increasing proportion of purely
male staminate flowers in an older umbel; (C) C L1 L2 L3
the plant as a whole has alternating phases of
being mainly male and mainly female, due to
an interaction of phenology within an umbel,
floral lifespan, and the timing of stigma recep-
tivity. (Modified from data using carrot (Dau-
0 8 16 24 32 40 48 56 64 72 80 88 96
cus carota) in Perez-Banon et al. 2007.) Flowering days of plant
30 • Chapter 2

A B C

sepal

ovule

petal

stamen

Figure 2.13 Types of flower symmetry and the associated flower diagrams: (A) typical actinomorphy, or radial sym-
metry; (B) typical zygomorphy, as in a labiate flower; (C) the curious symmetry of Dicentra flowers, with up/down,
rather than right/left, symmetry. There are five axes of symmetry on (A), and dotted line shows single axis of sym-
metry on (B). (Modified from Barth 1985.)

Table 2.5
Interpretations of Floral Symmetry

Planes of symmetry Symmetry type Synonyms Generic examples

Many Radial Actinomorphic, regular, Primula, Narcissus

multisymmetrical
Two Disymmetrical Biradial, bisymmetrical Dicentra
One Bilateral Zygomorphic, irregular,
bilabiate
 Right-left symmetry Bilabiate, medial zygomorphic Salvia, Corydalis
Upper-lower symmetry (No term in use)
None Asymmetrical
Floral organs in spirals Radial, actinomorphic, regular Nymphaea, Magnolia
 Left or right handed Enantiomorphic, enantiostylic Cassia, Solanum

Source: Modified from Neal et al. 1998.

fed upon by a whole range of visitors, and it has often trolled foraging, often working methodically around
been noted that beetles, flies, and lepidopterans par- the ring nectary or the series of nectaries, sometimes
ticularly favor radial flowers. Some of these land and with an appearance of counting a full circuit of petals
forage in a relatively disorganized or haphazard fash- or nectaries and leaving the flower after one full circuit
ion, but others, also including bees, show a more con- (fig. 2.14).
 Floral Design and Function • 31

50
Bombus
Apis
40

Frequency (%)
30

20

10
Figure 2.14 Apparent “counting” by bumblebees and
honeybees feeding on strawberry flowers (Fragaria) with a
radial design. Many bees sample just one or two nectaries,
but the majority sample all five and very few do more 0
than one full circuit (i.e., few sample more than five 1 2 3 4 5 6 7 8 9
times). (Data collected by Emily Clark and author.) No. of nectaries sampled

In contrast, bilateral shape allows the manipulation difficult to disentangle innate preference from previ-
of visitor approach so that the incomer is forced to en- ous visual experience here; West and Laverty (1998)
ter the corolla in a specific manner, which can in turn certainly found no preference expressed in naive
ensure appropriate passage past the anthers. Bilateral bumblebees.
flowers are nearly always oriented to open in a hori- There are some indications that bilaterality can ac-
zontal plane, and artificially changing their orientation celerate diversification and speciation in angiosperms
leads to reduced visits or a higher proportion of ille- (Sargent 2004), although this finding was only partly
gitimate visits or both, as Ushimaru et al. (2009) dem- supported in a later analysis (K. Kay et al. 2006).
onstrated with syrphid flies and Commelina flowers, Inflorescences often serve to turn bilateral individ-
attributing the effects to both poorer recognition and ual florets, which can gain the benefits of zygomorphic
poorer landing behavior. (However, it might be noted anatomy and visitor directionality, into an appearance
that something rather similar can happen in radial of radiality at least from a distance; this may give the
flowers: hummingbirds consistently approached from plant some of the benefits of both floral types. Exam-
a face-on direction for naturally horizontal Silene ples can be seen in several of the categories dealt with
flowers, but when the birds visited artificially fixed in section 2, Particular Floral Shapes, below.
vertical flowers, they arrived from the side and from
any compass direction, so contacting the sex organs in
random fashion [Fenster et al. 2009]). Nectar Spurs
Bilaterality is often combined with concealment of
the nectar, again ensuring that the visitor has to ap- A wide range of flowers from most of the architectural
proach appropriately and insert its head or tongue categories discussed in the next section have tubular
“correctly.” There are some indications that in bilateral extensions termed nectar spurs (plate 19 shows ex-
flowers a more perfectly symmetrical bilaterality is amples). Spurs may be formed from various different
also favored by visitors, perhaps because such sym- tissues, but most commonly they originate from pet-
metry indicates superior quality and strong develop- als; they may project from the back of the flower or
mental stability (Müller 2000). For example, bumble- may be tucked within it. They provide a very conve-
bees preferred symmetrical Epilobium flowers over nient way of offering a larger nectar reward without at
somewhat lopsided asymmetric forms (Müller 1995a). the same time filling up the corolla (which would
But Midgley and Johnson (1998) give examples of make this nectar available to inappropriately small or
visitors showing no such preferences, and it is always short-tongued visitors). Spurs have clearly evolved
32 • Chapter 2

repeatedly across most plant families (Hodges 1997), groove at its base leading to a nectary, so that visitors
and they can be up to 400 mm long in a Madagascan (mainly hawkmoths in this case) must hover and probe
orchid (Nilsson 1988). There is good evidence that almost vertically upward with their tongues, repeating
their appearance in a particular taxon can give a major the feat at each petal in turn.
boost to floral radiation and speciation (Hodges 1997; Pendant flowers may also help to protect the inter-
K. Kay et al. 2006; and chapter 11). There may be a nal organs from rain and weather-related damage, and
punctuated, fast change in spur length during specia- an interesting example here is Pulsatilla cernua, whose
tion episodes, since in columbines (Aquilegia) the flower stalk bends from erect to pendulous and back
spurs seem to have evolved rapidly at times to fit the again during anthesis (Huang et al. 2002). During the
adaptive peaks predefined by pollinators (Whittall and key period of pollen presentation, the pollen is pro-
Hodges 2007). tected from rain in the pendant flower; thereafter, as
In Aquilegia each of the petals normally has a visi- the petals elongate, they develop unwettable hairs so
ble backward-pointing spur (fig 8.2), producing a that the flower, once erect again, still protects its re-
revolver flower effect (see below). In contrast, Del- maining pollen.
phinium species (larkspurs), in the buttercup family,
have petaloid sepals, just one of which is elongated at
the underside of the flower into a long spur. Very long- Floral Shape Change
spurred species occur in the orchids, for example in
Platanthera, where pollinating moths only approach Some flowers show diurnal changes in shape and ac-
as close as they need for their tongue to reach to the cessibility, for example, opening wide in the daylight
end of spur; hence they effect much less pollination in and closing at night or during rain (e.g., Nemophila,
shorter-spurred individuals, giving ongoing selection Hepatica, Crocus) or more specifically, opening in re-
for increasing spur length. sponse to sun and closing fully or partly when it be-
The presence of nectar spurs can lead to conver- comes cloudy (e.g., Adonis, some Mesembryanthe-
gence within flowering communities. For example, the mum, some Gentiana). Bergeranthus flowers in South
South African flora has species from at least 10 differ- Africa open daily at about 1530 and close after about
ent plant families, including Ixia, Geissorhiza, and 3 hours, closely tied in to ambient temperatures above
Pelargonium, all with spurs around 90–100 mm in 23ºC (Peter et al. 2004), and they are almost exclu-
length and all visited by long-tongued nemestrinid and sively visited by bees during their opening hours. Gen-
tabanid flies (chapter 13). In Kenya a number of or- tians are particularly interesting because they may
chids converge on a white-flowered long-spurred pat- show two kinds of flower closure, one in response to
tern (Martins and Johnson 2007), and the hawkmoth environmental conditions (e.g., cooling temperatures
visitors have matching tongue lengths; in these cases or approaching thunderstorms [Bynum and Smith
the spurs contain a nectar concentration gradient that 2001]) and a second, more permanently in direct re-
may have adaptive significance (chapter 8). sponse to being pollinated (He et al. 2005). In the lat-
ter case, the closed flowers are often retained on the
plant for some time to add to the display effects. Fire-
Pendant Habit weed flowers (Chamerion angustifolium; syn Epilobi-
um) show a similar pollination-induced closure mech-
This is another common feature that may occur in any anism within 4 hours of pollen receipt (Clark and
flower design, but it is particularly common in bowl- Husband 2007); the time to close is reduced when pol-
and bell-shaped flowers (plate 4). A pendant habit ex- len loads are larger and perhaps increased when self-
cludes many visitor types because of the agility in pollen is deposited, indicating a consistently adaptive
flight and landing that is required to visit effectively response.
(either an ability to feed while clinging upside down or Less drastic shape changes, such as increasing re-
an ability to feed while hovering). A simple hanging flexion of petals or sepals, are also a common occur-
bell is a common structure, but more complex variants rence, and such changes often act as a signal of the age
do occur. For example, in Turk’s cap lilies (Lilium of an individual flower and hence perhaps the likeli-
martagon) each petal of the bell has a narrow flanged hood of pollen availability; an example of this effect
 Floral Design and Function • 33

was described for Anemonopsis visited by bumblebees Some examples within this type are more compli-
(Pellmyr 1988). cated. For example, hellebores have tubular petal nec-
Smaller shape changes may also occur within one taries within the bowl, concealing the nectar from
part of a flower, including elongation of the anthers or short-tongued visitors (plate 19B). Other genera con-
stigma linked to protandry or protogyny (chapter 3) tain pollen-only flowers, with no nectar on offer; Pa-
or altered curvature of these structures. Or there may paver is a classic example, but this situation is also
be subtle and reversible movements of parts of the common in Helianthemum, Adonis, and some species
flower, seen for example in the lateral (inward) move- of Cistus.
ment of anthers in Mahonia when the flower is stimu-
lated by physical contact from a visitor (plate 12B),
increasing the chances of pollen contact with animal Tubular Flowers with Radial Symmetry
surfaces.
Here the perianth parts are elongated and arranged at
their base to form the tube, while in the outer corolla
6. Particular Floral Shapes the petal tips are reflexed somewhat to form a flat-
tened landing area around and above the tube (plates 4
The listings below approximately follow the catego- and 6 show examples). The flowers typically have few-
rizing of flower types by Kugler (1970) and by Faegri er reproductive parts that are more fixed in number
and van der Pijl (1979), although with some simplifi- compared with more primitive disk and bowl flowers,
cations. Many schemes have been produced over the and they have regular and small numbers of petals or
years, some more strictly botanically correct, but the calyx lobes. This design leads to visual concealment
main requirement here is to distinguish types in rela- of the nectary, and as a result, the nectar can only be
tion to possible or actual visitors. reached by a visitor with a suitably elongate tongue.
Such flowers occur in many plant families, often where
the “typical” flower form is quite different.
Open Disk or Bowl Flowers This functional state can be achieved in several dif-
ferent ways (fig. 2.16). Elongation by uniting both se-
This simplest of flower types is extremely common pals and petals into separate tubes is the commonest
across many plant families (plates 2 and 3), with the form, and the corolla then usually has a narrow tubular
petals forming a relatively flattened disk when fully basal region, into which only visitor mouthparts can
open. The petals may be touching or overlapping later- be intruded, and a flat outer disk of petal tips, to offer
ally for much of the flower’s life but can become quite landing or gripping space. This design (plate 6) is very
separate and well spaced as the flower becomes fully familiar in flowers such as gentians (Gentiana), peri-
mature, giving a more star-shaped appearance (fig. winkles (Vinca), forget-me-nots (Myosotis), and prim-
2.15). In other cases the petals persist in a more raised roses (Primula), each of these examples being from a
orientation forming a deeper bowl, but still with very different family. The outer tube formed from the se-
free access to most visitors. pals acts as support and protection to the base of the
This kind of floral arrangement most commonly oc- corolla and may help protect against illegitimate nec-
curs with a single layer of four to eight petals, as in tar robbery from short-tongued visitors.
buttercups (Ranunculus), Anemone, Helleborus, pop- Uniting the petals into a tube that has little or no
pies (Papaver), and many rosaceous plants, such as support from sepals is also possible, as seen in honey-
bramble (Rubus), hawthorn (Crataegus), cherry (Pru- suckles (Lonicera, plate 16A) and many bellflowers
nus), or Potentilla. More rarely in wild plants (but (Campanulaceae, e.g., plate 4D); these examples gen-
rather commonly in garden hybrids) there are multiple erally have protected inferior ovaries and so need less
petal arrays, as seen in many Rosa species. These flow- physical protection from the sepals. Tropical versions
ers have a mass of anthers positioned centrally within are perhaps commoner and include Stephanotis (plate
the cup or bowl and have shallow exposed nectaries, 6H), Dipladenia, and Plumbago, the latter having a
so that both pollen and nectar are freely available to very narrow tube of fused blue petals and a calyx
visitors. bearing fine sticky hairs externally (plate 6G), perhaps
34 • Chapter 2

N
N
N

Ranunculus
Anemone Euphorbia Helleborus
N

N
N

Papaver Geranium Rubus

(no nectary)

B nectaries (N)
on receptacle

bract

petal

ovaries

sepal Brassica Anisodus

stamen

Potentilla

Celastrum

Capparis Malva

Figure 2.15 Various radial designs of flowers: (A) in cross sections, with the positions of nectaries indicated; (B) in
frontal view. Note that this design includes star shapes (often with petals and sepals alternating) and bowls or bells.
(Redrawn from Proctor and Yeo 1973.)

deterring ants (chapter 25). Red tube-shaped flowers Caryophyllaceae, especially in the genus Dianthus
are also common in bird-pollinated plants such as (pinks, campions, etc.). The sepals form a distinctive
Hamelia or Aloe (plates 26 and 27). tubular cup from which thin dissected petals emerge
Elongation by forming a sepal tube is an alternative and spread out to give a frilled effect.
approach and is characteristic of many plants in the In the Brassicaceae (a taxon usually with small and
 Floral Design and Function • 35

Convolvulus Nicotiana Polemonium Centropogon

Ericaceae Crassulaceae

Curcubitaceae Boraginaceae Lythraceae

Figure 2.16 Types of tubular design and how they are achieved, including elongate separate but overlapping, or
fused, petals (and sometimes sepals).

shallow cross-shaped flowers), some of the larger- the calyx tube. In some Geraniaceae species (e.g., herb
flowered genera, such as cuckoo flowers (Cardamine) robert, Geranium robertianum) and in some mallows
and wallflowers (Erysimum), have the four sepals (Lavatera, plate 3E) and Hibiscus (plate 3D), a similar
elongated and pressed tightly together (without actual design occurs, although with five or six sepals and pet-
fusion) to form the tube, while the four petals are sepa- als. In some of these examples the inner surface of the
rate and very narrow basally but expand apically above corolla effectively becomes ridged, producing a series
 Another Random Document on
Scribd Without Any Related Topics
 CHAPTER NINE
A Cry in the Night

Hours later, Ted lay awake in the upper bunk of the

double-deck bed he shared with Randy. The foam-
rubber mattress under him was soft as a cloud, and the
cool artificial air of the house inflated his lungs
satisfyingly.

But though he was comfortable, Ted could not sleep. He

had lain awake for an hour. He guessed it was because
of the excitement of the past few days and the fact that
this was his first night on solid ground after months of
life in space.

He climbed down the ladder to the floor, quietly so as 100

not to disturb Randy. He stared through the clear plastic
walls of his room at the hushed Martian night. The sky
was a glittering canopy of starlight. Phobos, the fleet
closer moon, cast a weak light over the landscape.
Beyond their desert back yard, Ted saw the dark
spreading mass of the sand bog which he had been
warned about. It was like quicksand and would draw
anything that touched it down to destruction. Ringing
the bog Ted saw thick clusters of white flowers, which
his father had said was a favorite food of the little
Martian color bears.

Ted had also learned that the animals fed at night. He

wondered if any of the creatures were in these parts,
and if there were any chance he would see one of them.
He kept his eyes on the bog for what seemed an hour,
but he caught no sign of movement down there. At last
his eyes grew blurry and he thought he could sleep. He
turned away and climbed the ladder.

Just as his lids closed, something startled him, and he

jerked up in bed. He wasn’t sure what had aroused him.
He sat there in the semidarkness, his heart bumping
rapidly, his ears alerted.

Then he heard a sound. It seemed far off. It was like a 101

wail, a cry. He came down the ladder again. In his
haste, he tripped on the bottom rung and went
sprawling. He turned anxiously toward the bed and saw
Randy sit up.

“I’m sorry, Randy,” Ted said. “I thought I heard

something outdoors.”
“I heard it, too,” Randy said.

The two looked outside, straining their eyes to pierce

the shadowy night. Suddenly Randy Whispered tensely,
“There!”

Ted stared where he pointed. There was a figure at the 102

edge of the bog. They heard the sound repeated. It
seemed to be coming from the moving figure. Ted
suddenly remembered his father’s field glasses lying on
a table in his parents’ room. Before going to bed, all of
them had used them to study the stars.

Ted tiptoed down the hall into his parents’ room.

Carefully he lifted the glasses from the table and
returned to his own room. He could hardly wait to train
the glasses on the mysterious thing beside the bog.

“Did you hear it again?” Ted asked as he swept his

glasses over the landscape.

Randy nodded. “It sounded like a color bear. He must

be in trouble.”

Finally Ted found what he was looking for. He was able

to make out a little furry body struggling at the bog’s
edge. The animal appeared to be trapped in the marsh.
One stubby paw was grasping a root growing out of the
bank. Ted handed the glasses to Randy.

“It’s a color bear,” Randy whispered. “He’s stuck in the

bog. He’ll never get out by himself.”

Ted saw a wistful look on Randy’s face. “I sure hate to 103

see anything happen to those little fellows. They’re so
friendly.”
“You mean they make good pets?” Ted wanted to know.

“They sure do,” Randy answered. “I owned one once,

until he fell into a bog. It seems they always end up in
one sooner or later.”

“I wonder if we could help him,” Ted suggested.

“It may be dangerous,” Randy warned. “If we should

slip....”

“You’ve been around them before, haven’t you?”

“Yes.”

“I’m willing to try it if you are,” Ted said.

“Let’s go then.”

“We’ll have to be careful not to wake the others,” Ted

said.

Softly they crept down the hall to the space-suit closet.

Silently they dressed and inflated their suits with
oxygen. Then they went through the air lock and on
outdoors.

Ted had brought a flashlight. The cone of whiteness 104

fanned out ahead of them, leading the way for them
over the red sands. As they drew near the sand bog,
the wails of the trapped animal became louder and
more frantic.

“We’d better hurry,” Randy said. “He may go down any

moment.”

They broke into a run and finally reached the side of the
little fellow. The only part of him visible now was his
round head, from which projected big cup-handle ears.
His short forepaws still clung to the root, but even now
the boys could see his grip loosening.

As they knelt beside him, they saw his violet button

eyes turned pleadingly up to them.

“The bank seems firm,” Randy said. “Let’s brace

ourselves and each take one of his paws.”

The black mud pulled strongly against them. After a few

moments the boys’ arms ached from the tug of war, but
they appeared to be winning the battle. Slowly the bear
rose out of his trap. Just as Ted thought his own arms
would be pulled off from the strain, the animal sucked
free of the clutching slime and came tumbling up over
Ted and Randy.

As the boys climbed to their feet, the color bear ran up 105
first to one and then to the other, and licked their
helmets gratefully with his long red tongue!
The little creature stood about two and a half feet tall
and was so roly-poly, he must have been nearly that
wide. The mud caked his body, some of it crawling like
thick molasses down into a black puddle around his flat
feet. He walked upright just as they did.

“What’ll we do with him?” Randy asked.

“Let him go, I guess,” Ted replied. “I wish we could 106

keep him, but I’m afraid Dad wouldn’t agree. For some
reason, he doesn’t like color bears. Besides, there’s no
place to keep him.”

They walked back toward the house. Presently Ted

turned and saw what he had feared. The bear was
trudging along behind. They tried to shoo him off. This
only made him hesitate momentarily and then start
following again. Finally they gave up, permitting him to
trail along at a distance.
When they reached the air lock, they opened the door.
As they waited for the pressure to come up, the color
bear stood outside looking in at them. Ted thought he
had the most plaintive expression he had ever seen. It
was almost human.

“We can’t let him stand out there like that all night,” Ted
said. “He might wake up the whole house with his cries.
They do cry, don’t they?”

“Just like babies,” Randy said.

“I forgot, though,” Ted said. “They can’t breathe our air

mixture, can they?”

“Yes, they can.” Randy told him. “They have a valve in 107
their bodies that takes care of that.”

“I believe we can wash that goo off him and leave him
in the kitchen until morning,” Ted said. “Maybe he’ll be
quiet if he’s clean.”

They let the bear in, and in appreciation he licked their

helmets again.

“If you want to stay in here, you’ll have to be quiet,”

Randy warned, just as though the animal could
understand.

“Hey!” Ted cried. “What’s wrong with him?” The little

animal was reeling around as though he could hardly
keep his feet, and his eyes were glazed.

“They always do that the first few times they enter our
atmosphere,” Randy answered.

The color bear adjusted himself quickly to the change

and then seemed all right again. Quietly the boys led
him down the hall toward the shower. In the bathroom
they shut the door, removed their helmets and turned
on the shower in a gentle spray. The bear did not take
to water willingly, and the boys had to force him under.
When he began squealing and kicking, Ted put his hand
over his mouth. As the little animal felt the warm water,
however, his broad mouth turned upward in a grin, and
he sat down in the middle of the plastic basin to enjoy
his bath.

While the mud was washing down the drain Ted began 108
to see what a beautiful creature the color bear really
was. His soft fur was white next to the body, then
merged into reddish brown at the tip. To make him even
more colorful, his paws, legs, and head had a bluish
tinge. “What a patriotic creature he would be on Earth,”
Ted thought. He had all the colors of the American flag.

When the animal was clean, Ted got out a blotting towel
that dried the bear in a matter of seconds. The little
fellow looked happy after his bath and grinned at them.
When he tried to lick their bare faces, they had to cover
up. He seemed hurt by their gesture and pouted for a
moment, with his lower lip quivering.

“See what I mean?” Randy said, grinning. “They’re

almost human.”

“I wish we could keep him,” Ted said longingly. “He

seems like lots of fun. I think I’ll ask Dad about it.”

As they were cleaning up the bathroom, Ted, who was 109

leaning over the shower basin, felt Randy’s hand press
sharply on his shoulder. Ted spun around. Standing in
the doorway was his father, a stern look on his face.
111
 CHAPTER TEN
School on Mars

“What in the world are you two doing?” Dr. Kenton

asked.

Ted told him the whole story of the rescue, ending up

with a request that they keep the Martian animal for a
pet.

Ted’s father shook his head. “That’s impossible. There’s

no place to keep him.” His face grew stern again. “You
two did a very foolish thing going out alone near that
bog. You might have fallen in. I want you to promise
that you won’t go near that place again.”

They promised. Ted knew it was no use arguing about

keeping the color bear. When his father made up his
mind, he rarely changed it.

As the three walked along the hallway with the bear, Dr. 112
Kenton said, “You kids woke me up with all that
splashing in the bathroom, but, fortunately, Mom is still
asleep. We must be quiet so that we won’t waken her
and Jill.”

The bear was reluctant to be forced out of the house

through the air lock. Ted knew the animal felt no worse
than he did. He had become quite attached to the little
fellow in even this short time.
When the bear was outside in the dark, he looked
mournfully through the transparent doors at his former
friends who had rejected him. Then he began wailing
softly. Ted looked hopefully at his father, wishing that he
would have a change of heart. But Dr. Kenton’s
expression was set, and Ted knew there was no chance
of the color bear coming back inside.

The three of them retired to bed, but Ted was a long

time getting to sleep. For almost an hour the Martian
creature kept up a soft wail. Ted covered up his ears
with his air-filled pillow, and he was finally able to drop
off to sleep.

The next morning Ted and Randy went to the front door 113
the first thing after they rose. There was no sign of the
color bear.

“I guess he finally gave up,” said Ted unhappily.

“I can’t understand his being alone like he was,” Randy

said. “Usually the little bears travel around in families of
about ten. I guess this one was an orphan.”

Hearing this, Ted felt even worse. “Maybe a wild animal

got him,” he murmured. “If it hasn’t already, it probably
will sooner or later. By the way, what kind of wild
animals do they have here?”

“None of them ever come close to the colony,” Randy

answered. “Hundreds of miles away, there’s the Great
Martian Forest where all kinds of them live. One of the
fiercest kinds are the elephant ants. Big herds of blue
rovers run across the desert closer by. There are
different kinds of birds here, too.”
“I’ve heard of a dangerous plant in the Great Forest,”
Ted said. “What’s it called?”

“The whip tree,” Randy answered. “It throws tentacles 114

around anything that’s near and draws it into its center
mouth.”

Realizing the dangers to the lonely little bear, Ted had

not much appetite for breakfast. Neither of the boys nor
Dr. Kenton had mentioned the adventure of the night
before, but Mrs. Kenton had heard some noises,
although they had thought she was asleep. She began
asking questions and finally got the whole story.

“I wish we could have kept that little animal!” Jill sighed.

“He sounds wonderful!”

“We can’t adopt every stray animal that comes along,”

Dr. Kenton said. “I’m sure the color bear will get back to
his family all right. He probably just strayed
temporarily.”

Dr. Kenton next said that he was going to report to the

science organization this morning. He asked the children
if they wanted to go along and register in school. They’d
have to within the next few days anyhow.

“Are the schools like they are back home?” Jill asked.

“They sure are,” her father said. “Just as modern as 115

you’ll find anywhere.”

Hearing this, the children were eager to go. Schools in

the twenty-first century were a combination of
wholesome entertainment and instruction. No dry
textbooks or cramped wooden desks with hard seats.
Ted and Jill had heard about the poor children of the
mid-1900’s who had to plod through school with such
handicaps as these, and they felt sorry for them.

Ted noticed that Dad seemed reluctant to leave Mom by

herself, but she did not seem to mind.

“Don’t worry about me,” Mrs. Kenton said merrily. “I’ll

have plenty to do unpacking our clothes and things that
they dumped in the living room yesterday. I won’t even
miss you four children!”

When the young folks and Dr. Kenton went outside in

their space suits, Ted saw that the sun was just a little
above the horizon. He had learned that men rose early
on Mars to take advantage of the warmth and
illumination of daylight.

Dr. Kenton looked into the purple sky through which the 116
stars gleamed. “It’s exactly six-fifteen now,” he said.

“How did you know that?” Ted asked in surprise. “You

didn’t look at your watch.”

“I didn’t have to,” his father answered. “That little disk

in the sky gives it to me.”

“That’s Phobos,” Ted supplied.

“Right,” his father answered. “It takes only six hours for
the moon to go from one horizon to the other, so you
can actually see its movement in a few minutes’ time.
By judging its distance from the star around it, I can get
the time.”

“That sure must take a lot of knowledge of the stars to

know just where each one should be at any one time!”
Ted said.
“It does,” the scientist replied, “but you’ll learn it in
school. I’ll bet Randy knows how to do it now. How
about it, Randy?”

“Yes sir,” Randy replied with a grin, “but I guess I’m a

little off after being away so long. I thought the time
was six-thirty.”

Dr. Kenton took another look, and Ted could see his face 117
redden inside his helmet. “I’m the one who’s a little bit
off, Randy!” he admitted. “It is six-thirty.”

Suddenly Jill cried, “Ooo—look!”

A half dozen large birds were swooping down on the

boat. Dr. Kenton did not appear alarmed—only amused.
“They won’t hurt us,” he said. “They’re whee birds and
very friendly.”

The beautiful birds folded their scarlet wings, tipped in

yellow, and perched on the sides of the boat. Then they
began giving out a peculiar, “Whee-whee,” as though
they were enjoying the boat ride.

“Don’t they sound funny!” Ted said.

The birds soared away as the boat turned into Main

Canal. A few minutes later, Dr. Kenton drove up to the
building they had registered in the day before. But
instead of docking at the building, Dr. Kenton continued
along the canal beside the building in the direction of
the other large building next to it.

“We’re going to the science building today,” the scientist

explained.
“Why is that as big as the administration building?” Jill
asked.

118
The birds soared away.
“Don’t forget, Jill, that science and research is our main 119
business on Mars,” Dr. Kenton told her. “Every
imaginable research project is carried on there. Your
schoolroom is there, too.”

Dr. Kenton docked the boat at the science building, and

the four got out and entered. When they had removed
their space suits, Dr. Kenton took the children to the
school superintendent’s office, where he left them. The
superintendent had them fill out cards, and then he
took them down a hall.

“We have only a hundred and fifty students enrolled, so

we don’t need many classrooms,” he said, and stopped
before one of the rooms, knocking on the door.

A dark-haired young man opened it, and the

superintendent introduced him to the children as their
teacher, Mr. Garland. He assigned the newcomers seats,
and since school had already begun for the day, he
went on with his lesson.

The room darkened, and a regular three-dimensional 120

color movie flashed on the screen. It was a picture
about the wonders of the Earth. Ted felt a lump rise in
his throat as he watched. What he was looking at was
the Natural Bridge in Virginia, not far from their old
home. Ted looked at Jill. A stray pencil of light from the
camera showed tears glistening in her eyes. Ted was
feeling a wave of homesickness himself. The wonders of
Mars were exciting, but there was no substitute in all
the universe for their own little plot of ground on Earth
where they had been born.

Ted was glad when the movie was over and another
subject was taken up. With slides, Mr. Garland
demonstrated the geography of Mars. Ted learned that
the red planet was mostly a vast stretch of desert
through which ran the marvelous network of canals. Mr.
Garland likened the climate of Mars to that atop a high
mountain on earth—the air thin and cold.

Ted was glad when the recreation period came and he

could exercise.

It was his first such opportunity since leaving Earth. In 121

the boys’ gym the athletic instructor was teaching the
game of basketball. Some of the students like Randy
had been born on Mars and knew nothing at all about
the game. Ted said that he had played a lot of it in
school back on Earth and volunteered to help the
instructor, who was glad of the assistance.

When school was out, the young Kentons and Randy

reported to the science-building office, where Dr. Kenton
was waiting for them.

“Did you get your assignment?” Jill asked.

“Yes,” he replied. “I’ll be leaving you in a few days.

We’re going on an expedition to Hellespontus, where
some mysterious fossils have been discovered. They
may be bones of the ancient Martians. If so, they could
solve the baffling riddle of what happened to those
remarkable canal builders.”

After getting into space clothes, they went to their boat

and started homeward. As they approached their
isolated house at the end of the winding watercourse,
Ted rose in his seat and pointed.

“Look!” he exclaimed. “There’s the color bear again!”

Sure enough, seated on the front doorstep, as though
waiting for them to return, was the little Martian animal
they had rescued the night before.

123
 CHAPTER ELEVEN
Yank

“Isn’t he the cutest thing!” exclaimed Jill, as she saw the

red-white-and-blue creature.

“I thought we were rid of him,” Dr. Kenton groaned.

He brought the boat to the end of the waterway and

tied it up. The children leaped out and ran to the bear,
who climbed to his chubby feet to greet them. He licked
the suits of Ted and Randy but merely stared at Jill and
Dr. Kenton.

“It looks like we just can’t get rid of him,” Ted said,
renewing his hope for possession of the animal.

“Oh, Father, can’t we keep him?” Jill pleaded, stroking

the color bear.

Randy patted the little round head, and the bear made a 124
sort of purring, contented sound as the children fondled
him.

Dr. Kenton threw up his hands helplessly. “I guess I

know when I’m licked!” he burst out. “If Mother agrees,
we’ll try and keep him. But you kids will have to attend
to him yourselves, and mind you keep him out of the
sand bog, or you won’t have him long.”
“We will!” Jill said. Now that she had made friends with
the bear, he seemed ready to accept her and licked her
suit as a sign of friendship.

Randy stayed outside with the bear while the other

children went inside to talk persuasively with their
mother. She objected at first, but finally yielded to their
persistence.

“We’ll have to make out a requisition for plastic material

for his outdoor house,” Dr. Kenton said. “Are you
children willing to chip in part of your allowance to pay
for it?”

They nodded.

“We’ll order it the same time as we do supplies for the

garden,” the scientist said.

“We’re going to have a garden?” Jill burst out. 125

“I thought we’d try it,” her father said. “That’s the only
way we can get fresh vegetables.”

When Dr. Kenton went to the study to make out the

requisition slip, Ted asked his mother, “Why didn’t Dad
want to keep the bear? It seems to me that he doesn’t
like those little guys, or is afraid of them, or something.”

“As a matter of fact, he is a little shy of them, I believe,”

she answered. “He accidentally hurt a baby one badly in
one of his explorations a few years ago, when he
crushed its forepaw under his boot and it ran off crying.
Your father’s so tender-hearted he’s probably reminded
of that painful incident every time he sees one of the
animals.”
“Maybe he’ll change after the bear has been around for
a while,” Jill put in.

The air-lock door opened, and Randy stuck his head in.

“We’d forgotten all about you, Randy!” Jill exclaimed.

“Are we going to keep him?” Randy asked anxiously. 126

“We sure are!” Jill piped. “Bring him in and let’s

introduce him to Mother.”

Randy let the color bear inside. When he began

staggering about, Mrs. Kenton exclaimed with horror:
“He’s dying, the poor little fellow.”

Randy assured her he wasn’t really—that he behaved

like this because of the extra oxygen in the air. Randy
said that before long the bear would be able to go in
and out without any bad effects at all.

Ted brought the animal over to his mother. She gingerly

patted his blue furry head. In response he licked her
dress. “Now we’re friends,” Mrs. Kenton said.

“We’ve got to give him a name,” Jill said. “What’ll we

call him?”

“How about Fuzzy?” suggested Mrs. Kenton.

“No. Teddy!” Jill said.

Ted wrinkled his nose. “Then you’d get him mixed up

with me. I think he ought to have a patriotic name
because of his colors.”

“How about Yank, then?” Mrs. Kenton said.

“That’s a good one!” Jill agreed. 127

“Yeah, that’s swell!” Ted said. “What do you think,

Randy?”

He shrugged and grinned. “It sounds all right to me, but

I don’t know what it means.”

Ted explained the word as being sort of a nickname for

America and Americans. Randy had learned quite a bit
about the United States flag, but the word Yankee was a
new one to him. After he learned its meaning, he
agreed that Yank was a perfect name for the color bear.
When Dr. Kenton returned, Ted felt that the final
introduction to the newest member of their family
should be made.

“Yank, meet Dr. Kenton,” Ted said formally.

Ted’s father smiled and approached the little animal.

“Hi, Yank,” he said.

His hand went out to pat the round head, but to

everyone’s surprise, Yank drew back with a cry of fright.
Dr. Kenton’s face went red as if he had been snubbed by
a human being. Ted felt sorry for his father. Did the bear
unconsciously know what the scientist had done to
another member of his kind?

“Don’t worry, John,” Mrs. Kenton said soothingly. “He’ll 128

come around to you before long.”

Her husband quickly changed the subject. “I’ve made

out the requisitions. I’ll send them over to headquarters
now on the video-sender.”
The children watched interestedly as he went to the
video-sender, which was connected to the radiophone.
He fastened the slips face down on a glass plate and
held open a switch for several seconds. About a minute
later, a buzz came over the radiophone.

“That means it’s been received,” Dr. Kenton said. “I 129

asked to have it sent to us tomorrow.”

“Why couldn’t you just phone it in?” Ted asked.

“This way there doesn’t have to be anyone on the other

end,” his father explained. “The requisition was handled
by an automatic machine.”

Yank was given temporary quarters in the basement. Dr.

Kenton said he could not live indefinitely inside like this
—that an outside shelter was absolutely necessary.
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