Table Of ContentRobin F.A. Moritz
Edward E. Southwick
Bees as Superorganisms
An Evolutionary Reality
With 76 Figures and 19 Tables
Springer-Verlag
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Budapest
Prof. Dr. Robin F.A. Moritz
Institute of Biology, Technical University of Berlin
Franklinstrasse 28/29, 1000 Berlin 10, FRG
Prof. Dr. Edward E. Southwick
Department of Biology, State University of New York
Brockport, NY 14420, USA
ISBN-13 :978-3-642-84668-7 e-ISBN-13 :978-3-642-84666-3
DOl: 10.1007/978-3-642-84666-3
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Preface
The honeybee (Apis melli/era L.) is one of the better
studied organisms on this planet. There are plenty of
books on the biology of the honeybee for all, the scientist,
the beekeeper, and the layman. In view of this flood of
publications one is tempted to ask: why does it require
another one? The answer is simple: a new one is not
required and we do not intend to present a new book on
"the honeybee". This would really just add some more
inches to the already overloaded bookshelf without sub
stantial new information. Instead, we intend to present a
book on the honeybee colony. This of course immediately
releases the next question: so what is the difference?
Although the difference may look insignificant at first
glance, we try to guide the reader with a fundamentally
different approach through the biology of honeybees
and eusocial insect societies in general. The biology of
individual colony members is only addressed when it is
necessary to explain colonial mechanisms, and the colony
as a whole, as a biological unit, which is the main focus of
this treatise. Both of us felt that all current textbooks on
bee biology put too much emphasis on the individual
worker, queen or drone in the colony. Often it is com
pletely neglected that the colony is a very significant
(if not the most significant) biological structure in bee
biology. It is only because eusocial insects live in colonies
that their ecological and economic impact are of so much
more consequence than that of any solitary insect.
The role of the colony has been recognized for a long
time giving rise to the term "superorganism" at the begin
ning of this century . Yet the holistic approach of these
early studies to understand complex colonies of social
insects failed. It had to fail because nothing was known
VI Preface
about communication, social control and the biological
processes that rule the colony. The rise of reductionism
and the study of individual intracolonial behaviour supplied
the data base which forms our current knowledge of the
biology of social insects. Though the reductionist
approach was, and still is, an important philosophical
pathway, it may sometimes constrain our view of biolog
ical mechanisms in complex systems. It is correct that
without a sound understanding of the simple mechanisms
we are bound to fail in understanding the more complex
system. Yet this does not mean that because we have
chosen to study simplicity in the first place, complexity is
of no interest anymore or cannot be studied. The opposite
is true. Based on the very detailed knowledge of individ
ual biology we are now in a position to construct a work
ing hypothesis for the more complex situations. It took
molecular biology several decades to grasp the link
between the genetic code and the physiological correlate
on the organismic level. In this book we want to take a
similar step from organismic to superorganismic biology.
Insect societies deserve much more attention and study
simply based on their ecological and environmental
importance and their prodigious biomass (which has been
estimated to be as much as one-third of the entire animal
biomass in the tropics, Wilson 1985). Colonies of ants,
bees, wasps and termites are responsible for considerable
turnover of materials, and they provide vast subject
matter for analysis.
We have chosen to focus on the colony of honeybees as
our central representative of all highly social colonial
insects. Being neither an individual nor a population it
whets oue appetite for exploration. Our studies of the
genetic, physiological, behavioural, and ecological charac
teristics of bee colonies point to the usefulness of treating
it as a biologically recognizable entity. We discuss the
convergent strategies that evolution and natural selection
has put together to make the superorganism as much a
functional unit for gene survival as any individual
metazoan.
If this book generates controversy and stimulates
students to conduct further work in the field of honeybee
biology, it has fulfilled its purpose. It is notintended as a
Preface vii
reference book on honeybee biology. It is meant as a new
conceptual framework of an "old" biological under
standing of the honeybee colony on the basis of modern
biological analysis and recent theories. Our book is
not the typical monograph of a species, covering all
aspects of its biology. Our goal is to present the honey
bee as it lives and thrives in its social unit, the colonial
superorganism.
This volume would not have been possible without the
advice, help and aid we received from several colleagues.
In particular we wish to thank M. Ayasse, M. Breed,
S.L. Buchmann, R.M. Crewe, M.J. Duchateau, H.
Esch, S. Fuchs, J.L. Gould, R. Hepburn, E. Hillesheim,
G. Koeniger, N. Koeniger, P. Kryger, M. Makela, D. W.
Roubik, J. Schmitz, P. Schmid-Hempel, M. Schwarz, J.
van der Blom, and H.H.W. Velthuis for many helpful
comments. However, we have not necessarily used all
their advice, and any errors that eventually will be found
in this volume are fully our responsibility. We are grateful
to N. Frisch for preparing the cover figure. Finally, we
wish to thank the Alexander von Humboldt Foundation
which enabled us to conduct cooperative research over
many years. This book evolved from these joint studies in
which we became dedicated to the idea that the individual
is interesting, but the group forms the central clue for
understanding the biology of colonies of social insects.
May 1992
Robin F.A. Moritz
Edward E. Southwick
Contents
Chapter 1 What Is a Superorganism? . . . . . . . . . . . . . 1
1.1 From Cells to Metazoan Organisms. . . . . . . . . . . . 1
1.2 What Makes a Social Group a Superorganism? .. 4
1.3 Diversity of Superorganisms . . . . . . . . . . . . . . . . . . 6
1.3.1 Termites................................. 7
1.3.2 Superorganismic Ants. . . . . . . . . . . . . . . . . . . . . . 10
1.3.3 Bees.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 12
1.3.4 The Naked Mole Rat ...................... 13
1.4 What Not to Expect from Superorganisms . . . . .. 14
Chapter 2 Evolution of Superorganisms . . . . . . . . . . .. 16
2.1 From Solitary Individuals to Superorganisms:
The Theories .............................. . 16
2.1.1 Darwin's Dilemma ....................... . 16
2.1.2 Individual Selection Models ................ . 17
2.1.2.1 Kin Selection ........................... . 17
2.1.2.2 Assured Fitness Returns. . . . . . . . . . . . . . . . .. 19
2.1.2.3 Parental Manipulation. . . . . . . . . . . . . . . . . . .. 21
2.1.2.4 Mutualism and Reciprocal Altruism . . . . . . .. 22
2.1.2.5 Testing Theories. . . . . . . . . . . . . . . . . . . . . . . .. 24
2.1.3 Group Selection. . . . . . . . . . . . . . . . . . . . . . . . . .. 25
2.1.3.1 Classical Group Selection. . . . . . . . . . . . . . . .. 25
2.1.3.2 Competitive Group Selection. . . . . . . . . . . . .. 27
2.1.3.3 Colony-Level Selection. . . . . . . . . . . . . . . . . .. 29
2.1.3.4 Testing Theories of Group Selection. . . . . . .. 30
2.2 From Solitary Individuals to Superorganisms:
The Evidence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 30
2.2.1 Sociality in Bees. . . . . . . . . . . . . . . . . . . . . . . . . .. 30
x Contents
2.2.2 Solitary and Subsocial Bees. . . . . . . . . . . . . . . .. 31
2.2.2.1 Megachile rotundata: The Individualist. . . . .. 31
2.2.2.2 Carpenter Bees: The Hierarchists . . . . . . . . .. 33
2.2.3 Primitively Social Bees. . . . . . . . . . . . . . . . . . . .. 35
2.2.3.1 Exoneura bicolor Smith: The Mutualist. . . .. 35
2.2.3.2 Halictine Bees: Getting Social. . . . . . . . . . . .. 38
2.2.3.3 Bombus: Controlling Environment. . . . . . . .. 41
2.2.4 Superorganismic Bees. . . . . . . . . . . . . . . . . . . . .. 44
2.2.4.1 Stingless Bees. . . . . . . . . . . . . . . . . . . . . . . . . .. 45
2.2.4.2 Evolution Within the Genus Apis . . . . . . . . .. 50
Chapter 3 Physiology ........................... 57
3.1 Development............................... 57
3.1.1 From Egg to Adult. . . . . . . . . . . . . . . . . . . . . . .. 57
3.1.2 Caste. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 59
3.1.3 Birth, Aging, and Death of a Superorganism .. 62
3.1.3.1 Birth................................... 62
3.1.3.2 Aging and Age Variation. . . . . . . . . . . . . . . .. 63
3.1.3.3 Death and Immortality. . . . . . . . . . . . . . . . . .. 65
3.2 Glands and Secretions. . . . . . . . . . . . . . . . . . . . . .. 67
3.2.1 Endocrine System. . . . . . . . . . . . . . . . . . . . . . . .. 67
3.2.2 Exocrine System .......................... 68
3.3 Feeding and Digestion. . . . . . . . . . . . . . . . . . . . . .. 69
3.3.1 Nutrition................................. 69
3.3.2 Food Exchange and the Meniscus Effect. . . . .. 70
3.3.3 Pollen Stores ............................. 72
3.3.4 Making Honey. . . . . . . . . . . . . . . . . . . . . . . . . . .. 72
3.4 Respiration ................................ 73
3.4.1 Respiration in Individuals. . . . . . . . . . . . . . . . .. 73
3.4.2 Respiration in Colonies .................... 73
3.5 Circulation................................. 74
3.5.1 Haemolymph Circulation. . . . . . . . . . . . . . . . . .. 74
3.5.2 Circulation in the Colony. . . . . . . . . . . . . . . . . .. 75
3.6 Colonial Excretion and Water Balance. . . . . . . .. 76
3.7 Metabolic Physiology. . . . . . . . . . . . . . . . . . . . . . .. 80
3.7.1 Temperature Control. . . . . . . . . . . . . . . . . . . . .. 80
3.7.1.1 Cooling................................ 84
3.7.1.2 Heating. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 86
Contents xi
3.7.1.3 Maintenance of Nest Temperature. . . . . . . .. 87
3.7.1.4 Optimal Environmental Temperature
and Nest Choice. . . . . . . . . . . . . . . . . . . . . . . .. 94
3.7.2 Mass-Metabolism Relationships and Colony
Fitness. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 95
3.7.3 Seasonal Relationships. . . . . . . . . . . . . . . . . . . .. 98
3.8 Neurophysiology. . . . . . . . . . . . . . . . . . . . . . . . . . .. 99
3.8.1 Vision ................................... 100
3.8.2 Chemical Sense ..................... . . . . .. 101
3.8.3 Acoustic and Mechanical Reception. . . . . . . . .. 102
3.8.4 Special Sense, Learning and Integration ...... 104
3.9 Muscle Function ............................ 105
3.9.1 Locomotion and Flight ..................... 105
3.9.2 Stinging and Biting ........................ 106
3.10 Circadian Rhythms and Sleep. . . . . . . . . . . . . . .. 107
3.10.1 Cyclic Metabolism ........................ 107
3.10.2 Cyclic Locomotion ....................... 108
3.10.3 Cyclic Ventilation ........................ 108
3.10.4 Sleep ................................... 109
Chapter 4 Communication Network
of the Superorganism . . . . . . . . . . . . . . . . .. 110
4.1 The Analysis of Communication Networks ..... 110
4.2 Division of Labour. . . . . . . . . . . . . . . . . . . . . . . . .. 112
4.3 Food Procurement
and Temperature Regulation ................. 114
4.3.1 The Search for Food. . . . . . . . . . . . . . . . . . . . . .. 114
4.3.1.1 Individual Search Pattern of a Scout ........ 114
4.3.1.2 Foraging a Patch of Flowers ............... 115
4.3.2 Communication Mechanisms ................ 116
4.3.2.1 Round Dance ........................... 116
4.3.2.2 Waggle Dance ........................... 116
4.3.2.3 Acoustic Signals. . . . . . . . . . . . . . . . . . . . . . . .. 118
4.3.2.4 Odour Signals. . . . . . . . . . . . . . . . . . . . . . . . . .. 119
4.3.2.5 Dorsoventral Abdominal Vibration (DVAV)
Dance .................................. 121
4.3.3 Central Food Handling and Social Integration 121
4.3.3.1 Amoeboid Foraging Pattern ............... 122
xii Contents
4.3.3.2 Nectar Storage. . . . . . . . . . . . . . . . . . . . . . . . .. 124
4.3.3.3 Queueing. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 124
4.3.3.4 Comb Utilization. . . . . . . . . . . . . . . . . . . . . . .. 125
4.3.3.5 Water Handling ......................... 125
4.4 Search for Housing. . . . . . . . . . . . . . . . . . . . . . . . .. 126
4.4.1 Nest Site Selection ......................... 126
4.4.2 Swarm Orientation ........................ 127
4.4.3 Migration ................................ 129
4.5 Pheromones.................. . . . . . . . . . . . . .. 131
4.5.1 Superorganismal Control ................... 131
4.5.2 Queen Pheromones Inside the Nest .......... 132
4.5.2.1 Queen Retinue Behaviour ........ . . . . . . .. 132
4.5.2.2 Colony Stabilization and Ovary Suppression
in Workers. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 133
4.5.3 Queen Pheromones Outside the Nest ........ 135
4.5.3.1 Swarm Attraction ........................ 135
4.5.3.2 Sex Attractant. .......................... 135
4.5.4 Worker Pheromones ....................... 136
4.5.4.1 Orientation . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 137
4.5.4.2 Colony Defence ......................... 138
4.5.5 Other Pheromones and Odours .............. 140
4.6 Learning ................................... 141
4.7 Social Intelligence and Network Analysis ....... 142
4.7.1 Social Intelligence ......................... 142
4.7.2 Network Analysis ......................... 143
Chapter 5 Ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 152
5.1 Demography of Natural Populations ........... 152
5.1.1 Life History Strategies ........ . . . . . . . . . . . .. 152
5.1.1.1 Sessile Phase . . . . . . . . . . . . . . . . . . . . . . . . . . .. 152
5.1.1.2 Mobile Phase ........................... 159
5.1.1.3 Life Cycle .............................. 160
5.1.2 Spatial and Temporal Distribution. . . . . . . . . .. 162
5.1.2.1 Colony Defence ......................... 163
5.1.2.2 Removal of Debris and the Dead .......... 165
5.1.2.3 Home Range ............................ 166
5.1.2.4 Mating Distance. . . . . . . . . . . . . . . . . . . . . . . .. 167
5.1.2.5 Overdispersion of Colonies ................ 168
