Emergent Properties

of Individual Organisms
Emergent Properties
of Individual Organisms

Christopher J. Paradise, PhD

A. Malcolm Campbell, PhD
Emergent Properties of Individual Organisms
Copyright Christopher J. Paradise and A. Malcolm Campbell. 2016.

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 Abstract
This book begins by describing what an individual organism is, compar-
ing preconceptions of the individual to non-standard ways of thinking
about individuals. Variation in what individuals are is described, using
giant fungi, clonal trees and honey bee hives as examples. Individuals
are thus shown to be emergent properties. Other emergent properties
of individuals are also described. Classic experiments that elucidated the
source of emotions in humans and other mammals are described. Emo-
tions arise from the actions of the nervous and endocrine system and
often include a variety of signals given to other individuals of the same or
different species. In particular, this book focuses on fear and anger, two
emotions that are closely related and often confused, but that have been
well studied. In one final example of emergent properties of individuals,
cooperative behavior is analyzed. The behaviors displayed by individuals
that facilitate cooperation among individuals and why those individuals
may actually cooperate instead of compete when acquiring resources or
defending against predators are discussed.

Keywords
fungus, superorganism, behaviors, natural selection, fight-or-flight, divi-
sion of labor, dominance hierarchy, subordinate, fear, anger, individual,
colony, physiological response, endocrine system, nervous system, coop-
eration, mutual benefit
 Contents
Preface...................................................................................................ix
Acknowledgments....................................................................................xi
Introduction.........................................................................................xiii
Chapter 1 The Definition of the Individual Can Be Stretched
Beyond the Classic Definition1
Chapter 2 The Nervous and Endocrine Systems Are the Sources
of Emotions.....................................................................17
Ethical, Legal, Social Implications: There Are Issues
With Using Prescription Drugs to Normalize
Behavior in Children26
Chapter 3 Individuals of Some Species Cooperate With Each
Other for Mutual Benefit.................................................29
Conclusion............................................................................................43
Glossary................................................................................................45
Index....................................................................................................47
 Preface
This book about emergent properties of individual organisms is part of
a thirty book series that collectively surveys all of the major themes in
biology. Rather than just present information as a collection of facts, the
reader is treated more like a scientist, which means the data behind the
major themes are presented. Reading any of the thirty books by Paradise
and Campbell provides readers with biological context and comprehen-
sive perspective so that readers can learn important information from a
single book with the potential to see how the major themes span all size
scales: molecular, cellular, organismal, population and ecologic systems.
The major themes of biology encapsulate the entire discipline: informa-
tion, evolution, cells, homeostasis and emergent properties.
In the twentieth century, biology was taught with a heavy emphasis
on long lists of terms and many specific details. All of these details were
presented in a way that obscured a more comprehensive understanding.
In this book, readers will learn about emergent properties of individu-
als and some of the supporting evidence behind our understanding. The
historic and more recent experiments and data will be explored. Instead
of believing or simply accepting information, readers of this book will
learn about the science behind emergent properties of individuals the
way professional scientists dowith experimentation and data analysis.
In short, data are put back into the teaching of biological sciences.
Readers of this book who wish to see the textbook version of this
content can go to www.bio.davidson.edu/icb where they will find
pedagogically-designed and interactive Integrating Concepts in Biology
for introductory biology college courses or a high school AP Biology
course.
 Acknowledgments
Publishing this book would not have been possible without the generous
gift of Dr. David Botstein who shared some of his Breakthrough Prize
with co-author AMC. Davids gift allowed us to hire talented artists (Tom
Webster and his staff at Lineworks, Inc.) and copyeditor Laura Loveall.
Thanks go to Kristen Mandava of Mandava Editorial Services for project
management and guidance. In particular, we are indebted to Katie Noble
and Melissa Hayban for their many hours and attention to detail.
Kristen Eshleman, Paul Brantley, Bill Hatfield and Olivia Booker
helped us with technology at Davidson College. We are grateful to ad-
ministrators Tom Ross, Clark Ross, Carol Quillen, Wendy Raymond,
Verna Case, and Barbara Lom who had confidence in us and encouraged
us to persist despite setbacks along the way.
Thanks to my wife Amy Brooks for her constant support during the
development of this textbook, and my daughter Evelyn for her endless
energy. Thanks to Malcolm Campbell for his steadfast resolve and opti-
mism. Without him, this book would not exist. Thanks to collaborator
Laurie Heyer for taking my sometimes half-baked math ideas and turn-
ing them into powerful and elegant Bio-Math Explorations. I learned a
lot from both of them. While the math is largely absent from this book,
our collaboration with her made this a better book. Nancy Stamp at
Binghamton University, and Bill Dunson and Richard Cyr at The
Pennsylvania State University influenced me greatly in how I think as
a scientist and approach my teaching. Finally, I thank my students in
Integrated Concepts in Biology II, who enthusiastically participated in
our experiment to redesign introductory biology, starting with the text
and ending with a new approach to teaching biology.
 Introduction
Ren Descartess famous quote, I think, therefore I am, is a powerful
statement on emergent properties. A human exists because they have
consciousness and can think. The human brain can be described in terms
of cellular functions and biochemical reactions. Yet describing the brain
does not explain the emergent property of human consciousness. Brains
perform at a level that exceeds the functions of individual neurons. Truly,
who could have predicted that consciousness would arise from all the
components that make up the human brain? Many other aspects of in-
dividuals, including the individual itself, can be considered emergent
properties.
In this book, several ideas about properties of individuals that lead
to emergence of new and unpredictable properties will be explored. In
the first chapter, in line with Descartes, the definition of the individual
will be contemplated, especially in cases when the lines of individuals
are blurred. The second chapter addresses a topic very familiar in daily
life but rarely studied in biology classes. Data will be used to help un-
derstand the biological origins of emotions. The final chapter explores
another topic debated by biologists, which is the conditions under which
organisms cooperate with each other.
 CHAPTER 1

The Definition of the

Individual Can Be Stretched
Beyond the Classic
Definition

A commonly held understanding of an individual organism may be clear:

All of the cells of mammals, for instance, define self by displaying pep-
tide fragments from every protein produced inside all of the cells of an
individual. We define an individual as a set of cells that display the same
message regarding what is the self. But we need a more general defini-
tion to apply to a wide range of organisms. As commonly used, the term
individual refers to an object that is indivisible (that is, a singular thing
separate from other singular things). All of the parts within the boundar-
ies of this singular object are indivisible. Multicellular organisms are indi-
viduals if the cells, tissues, and organs that make up the organism cannot
survive on their own. There may also be a genetic requirement in that an
individuals cells are all composed of the same genome.
Questions about what an individual organism is have been debated
by biologists for years. Considered from the standpoint of an animal,
it seems quite clear that an individual is composed of all the cells, tis-
sues, and organs contained within the epidermis of that animal. However,
there may be biological entities whose status as individual organisms is
far from obvious, making the question not so easy to answer. This may
challenge ones conception of just what is an individual. It also illuminates
the emergent property of the individual arising from a collection of cells.
James Anderson and his colleagues studied several species of fungus in
Michigan (Smith et al., 1992). One species is called Armillaria gallica, or
2 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

the honey mushroom. One of their goals was to determine the size lim-
its of individuals. This species of fungus, like many others, is a decom-
poser and survives on wood. Anderson and his colleagues sampled for the
fungus in a forest. To understand the results of the study, it is helpful to
know a few things about fungi. Many fungi live in the soil and are only
noticed when they produce fruiting bodies, also known as mushrooms
(Figure 1A). Mushrooms are the enlarged aboveground fleshy fruiting body
of certain types of fungi. The part that lives underground is composed of
microscopic thread-like structures called hyphae (Figure 1B). The branch-
ing growth pattern of hyphae leads to development of a mycelium, which
is an interconnected network of hyphae. An important aspect of the life

Figure 1 Fungi. A, Armillaria gallica mushrooms. B, Fungal hyphae.

Source: A, http://en.wikipedia.org/wiki/Armillaria_gallica#mediaviewer/File:Armillaria_
gallica_26659.jpg, Author: Dan Molter. This file is licensed under a Creative Commons 3.0
attribution license. B, http://en.wikipedia.org/wiki/Mycelium#mediaviewer/File:Hyphae.JPG,
Author: TheAlphaWolf. This file is licensed under the Creative Commons Attribution-Share
Alike 3.0 Unported license.
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 3

cycle of Armillaria species is the formation of rhizomorphs, aggregations of

hyphae that transport resources and materials.
Fungi can reproduce sexually, but most fungi do not have readily
recognizable males and females. Basidiomycota, the group to which
Armillaria belongs, have haploid mycelia. Many fungi also have self-
incompatibility. The honey mushroom has two self-incompatibility
loci. Two individuals are reproductively compatible only if they have
different alleles at each self-incompatibility locus. If the mycelia of two
individuals are compatible, they fuse and swap nuclei. Two compatible
nuclei remain in pairs for a time. When nuclei do fuse a diploid cell is
formed, which quickly undergoes meiosis to produce four haploid nu-
clei that each migrate into a structure called a basidiospore, which are
often produced on mushrooms. The resulting haploid mycelia are called
mating types. Fungi can also reproduce asexually, through vegetative
growth of mycelia.
Anderson and his colleagues placed wooden tongue depressors in
the forest soil along two 1 kilometer transects, one oriented north/south
and the other east/west. Hyphae of the wood-decomposing fungi quickly
colonized these sticks. After a period of time, the researchers collected the
tongue depressors and cultured the fungi. In addition, they made cultures
from mushrooms and rhizomorphs that they collected from soil pits and
mycelia they collected from under the bark of trees. The scientists used
several methods to discriminate between honey mushroom individuals.
The scientists determined the self-incompatibility alleles of fungal
cultures. They also determined the patterns of DNA fragments that were
produced when mitochondrial DNA was chopped up using restriction
enzymes to produce fragments of varying length that were then separated
on gels. The self-incompatibility loci and mitochondrial DNA loci are
known to have multiple alleles in the honey mushroom. The researchers
reasoned that if the collected fungi were all from the same individual,
they would only see four mating types in haploid mycelia and mush-
room spores. This pattern would also be possible in an inbred population,
but in that case, the restriction enzyme data would show a low degree of
variation in the mitochondrial DNA. If more than two alleles were found
at a single locus among the fungal samples, then that would also indi-
cate more than one individual was present. Anderson and colleagues also
4 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

used random amplification of polymorphic DNA (RAPD) to look for

heterozygosity in nuclear genetic loci. In RAPD, segments of DNA are
randomly amplified using polymerase chain reaction (PCR) primers. The
scientists used three primers, and each amplified more than one fragment
of DNA, which was either present or absent in different haploid cultures.
Again, a high degree of similarity among haploid cultures sampled from
different locations would be indicative of inbreeding, as opposed to a
single individual.
Anderson and his colleagues found only two alleles in each of five
loci digested by restriction enzymes in all fungal samples from one large
area of the forest, which they denoted as individual 1. Each of the fungal
samples from this same area contained all of the 11 RAPD sequences,
although not all 11 were evident in each haploid sample. Twenty more
RAPD and 27 RFLP from samples of diploid tissues in the individual 1
area were tested further and found to be identical across samples. Samples
from what the scientists denoted as individual 2 were found to have
only one allele at each of two restriction enzyme loci and lacked five of
the RAPD fragments found in individual 1. From the distribution of
the samples that showed similar genetic structures from multiple analy-
ses, Anderson and colleagues estimated the boundaries of these different
individuals.
One individual fungus can produce only four possible mating types.
Because there are two loci and each is always heterozygous, meiosis pro-
duces four haploid cells from one diploid cell and each contains one of
two alleles at each locus. However, with more than two alleles, many
compatible mating types are possible. Anderson and colleagues only
found two alleles at each self-incompatibility locus from samples over a
wide area, leading to the possibility that these samples were from the same
individual. The RFLP and RAPD data helped support the conclusion
that these samples were all from the same individual. Only two alleles
were found in each restriction enzyme locus in all samples found within
the individual 1 boundary, further supporting the conclusion that only
one individual was present.
The genetic signature of samples from the individual 2 area were dif-
ferent from those of individual 1, which allowed Anderson and colleagues
to clearly demarcate the southwestern boundary of individual 1. Had they
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 5

sampled further north and east, they might have discovered the full extent
of individual 1s boundary. Although Anderson and colleagues discov-
ered several large A. gallica individuals, the largest was estimated to cover
15 hectares. All of the fungal samples collected from this area had the
same mating type, similar mitochondrial DNA restriction patterns, even
if individual haploid cultures were not exactly the same, and the same
11 RAPD fragments. Because of the variation among individual haploid
cultures, the researchers knew that each of these loci were heterozygous in
the diploid condition, allowing them to reject the hypothesis that these
samples were from different but closely related individuals.
Anderson and colleagues next set out to estimate the biomass and
age of the largest individual, individual 1. To estimate age, the scientists
had to estimate the rate of expansive growth outward from the center.
They assumed that the rate of growth was constant, which allowed them
to back-calculate to determine how long it took individual 1 to expand
to its current size. They used three methods to estimate the growth rate
(Table 1). Anderson and colleagues measured the maximum linear growth
of rhizomorphs along wooden stakes during one growing season. The sci-
entists also measured the maximum growth rate of cultures in the labora-
tory at different temperatures. To estimate mass, the scientists collected
soil samples, carefully separated fungal rhizomorphs from roots and soil,
dried the material, and weighed it to obtain the biomass per unit area of
soil. The wet mass was also estimated.
Anderson and colleagues knew that soil temperatures in the forest
ranged from 14o C to 16o C for about 90 days per year; and the rest of

Table 1 Estimates of growth and size of large

A. gallica individual fungus.
method maximum growth rate
wooden stakes in forest soil
19.7 3.1 cm/year
(average of ten longest out of 45)
laboratory cultures at 12C 0.0 mm/day
laboratory cultures at 15C 2.1 mm/day
laboratory cultures at 22C 4.7 mm/day
biomass (dry mass) 6.25 g/m2
wet mass 64.4 g/m2

Source: From Smith et al., 1992, Figure 1 legend.

6 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

the year, temperatures were below 14o C. They then calculated the an-
nual growth rate of laboratory cultures using the daily growth at 15o C
for 90 days, which is 0.189 m/year (2.1 mm/day * 90 days * 1 m/100 mm).
This is quite comparable to the annual growth on wooden stakes in the
forest soil (0.197 m/year). If this individual fungus grows in all direc-
tions at the same rate from a central point, it would be circular, and the
maximum distance across would be the diameter of the circle. The ra-
dius is half of that, which is the maximum distance it grew during its
life. If it grew steadily at 0.193 m/year (the average of the two estimates
made by the scientists), then this fungus is 1,645 years old [(635 m/2)/
(0.193 m/year)]! Anderson and colleagues argued that this may actually
be an underestimate of the age of the fungus, because competition with
other honey mushroom individuals would slow growth, as would adverse
climate conditions (such as, cold growing seasons).
The wet mass of the honey mushroom in the Michigan forest was
calculated based on the average wet mass estimate of 64.4 g/m2. First
convert the area to hectares, using the conversion of 10,000 m2/hectare.
Second, convert grams to kilograms by dividing by 1,000. Finally, multi-
ply by 15 hectares, which is the estimated area occupied by individual 1,
to obtain 9,660 kg. That is 9.66 metric tons, and when Anderson and
colleagues multiplied that by 10 to obtain the estimated total fungal mass,
they obtained 96.6 metric tons, which is close to the mass of an adult blue
whale! This may well alter perception of what an individual is. This one
individual fungus likely grew vegetatively for centuries to become a very
old and large individual.
Not all fungi grow to this size; in fact, most are much smaller and
often multiple individuals of the same species live in the same soil, un-
like the situation with the honey mushroom. But individuals of other
species of fungi have been shown to achieve sizes of the magnitude of the
honey mushroom individual, so it is not uncommon. A phenomenon
about fungal growth is that it is dynamican individual can lose mass
in one area and regrow it later. Fungal tissue is not as highly integrated as
the tissues of a blue whale. The property of the individual emerges from
the hyphae, mycelia, and rhizomorphs that make up the individual, and
in this instance that individual occupies space that no other honey mush-
room can occupy.
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 7

Some scientists have questioned whether this enormous individual

that Anderson and colleagues found is actually an individual. They
claim that more empirical information is necessary, including whether
or not rhizomorphs in one part of the forest are actually connected to
rhizomorphs in another part of the forest. This may reveal something
about the concept of the individual; if the fungus is an individual, then
the boundaries of an individual do not necessarily have to be contained
within a single outer layer that we can perceive. The property of being
an individual emerges as more than the sum of the parts. Indeed, when
studying plants ones perception of the boundaries of an individual may
be biased by what is seen aboveground. But the patterns in aboveground
structures may suggest clues. For instance, quaking aspen (Populus tremu-
loides) often grows in distinct stands, with trunks in the middle larger
and taller than trunks towards the exterior. This pattern may result from
growth of a single individual or production of seeds that do not disperse
far from the parent.
Karen Mock and her colleagues tested the hypothesis that the trunks
in stands of quaking aspen belonged to a single individual (DeWoody
etal., 2008). They sampled stems from aspens in an aspen forest in central
Utah (Figure 2). Each of 209 sampled trunks was the closest to the center
point of a square in a grid of 50 m 50 m squares. If no stem was within
5 meters of the center point, no sample was taken in that square. This
sampling scheme allowed them to systematically sample the entire extent
of the forest but not have to sample every tree.
At each trunk, the researchers collected a tissue sample. DNA was
isolated and assayed for seven microsatellite loci (Table 2). Microsatellite
DNA is a repeating sequence of one to six base pairs of DNA. For in-
stance, the sequence cytosine-adenine (CA) may repeat, and the number
of times it repeats varies among different alleles. The high number of al-
leles present at microsatellite loci leads to many possible genotypes within
a species, making them very useful for population genetics studies.
At each locus in each sample, the scientists determined the size of the
repeated microsatellite DNA sequence, which let them identify the allele.
CACACACA could be distinguished from CACA, for instance, based on
size. The genotype of a particular stem is the set of alleles present at the
seven microsatellite loci. The researchers mapped the genotypes on an
8 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

Figure 2 Aerial photograph of aspen forest sampled by Mock and

colleagues (circled area).
Source: Image from Google Earth.

Table 2 Genetic analysis of quaking aspen stand in Utah.

Sample size was 209.
variable value
number of distinct genotypes 46
number of samples containing the most common genotype 141
number of samples containing genotypes differing from
5
most common genotype by a single allele
number of samples containing genotypes differing from
63
most common genotype at between 4 and 7 alleles
estimated area covered by most common genotype 43.6 hectares

Source: From De Woody et al., 2008, text.

aerial photograph of the site. One genotype was found in a majority of

samples. The extent of the distribution of this genotype was compared to
a boundary of trunks that had the same phenotype, determined from a
different study.
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 9

Mock and her colleagues concluded that there were up to 41 individ-

ual aspen in this forest, which is far fewer than the 209 stems sampled.
Most of the forest was made up of just one individual. Although they did
not sample the entire forest and could not determine the extent of the
other individuals, none of them could be as large as this one, based on
the total size of the aspen forest. The researchers concluded that all 141
trunks with the same genotype plus the five trunks that differed from the
dominant genotype at only one allele belonged to the same individual,
because the probability of seeing identical genotypes in two unrelated
individuals is very small. In the case of microsatellites, it is reasonable
to assume that the researchers picked loci that are on different chromo-
somes, and thus the probability of an individual getting a particular mic-
rosatellite allele is independent of getting a particular allele at a different
genetic locus.
Even if two loci are on the same chromosome, they would try to pick
microsatellites that are separated by enough DNA that the two loci are
rarely inherited together. They also knew that there were more than 2 al-
leles at each locus, up to 20 in some cases. While this makes the determi-
nation of the probability of obtaining the same alleles at each locus more
difficult, if one were to obtain the same alleles at each locus, it would be
highly likely that the two samples would be from the same individual.
If one assumed there were only two alleles at each locus, and each
one occurs with probability , the probability that two individuals have
thesame genotype at a particular locus is the probability of matching on
one chromosome times the probability of matching on the other chromo-
some, which is 1/2 1/2 = 1/4. They then raised that probability to the
power of 7 because there were 7 microsatellite loci tested. This yields a
probability of (1/4)7 6 1025 in the case of two equally likely alleles
at each locus.
However, because the researchers knew there were multiple alleles at
each locus, their probability estimates were much lower than that, on the
order of 1 10210. Because most microsatellites have at least five alleles,
the chance of identical genotypes in two randomly selected unrelated in-
dividuals is extremely small.
Based on a similar probability calculation, Mock and her colleagues
further concluded that the five trunks that differed by one allele were part
10 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

of the same individual but had undergone a mutation while growing

vegetatively. The samples that differed by four to seven alleles were from
40 different individuals found in 63 trunks. Some of these individuals
were single stems, but some were made up of several trunks.
Aspen can grow vegetatively by sending up new trunks from roots
that spread out along the ground. They can also reproduce sexually, but
this type of asexual reproduction leads to many trunks that are all identi-
cal to each other genetically and phenotypically. The trunks are all con-
nected by an extensive root system. According to researchers, the large
aspen clone in central Utah is the largest individual organism on the
planet, at least the largest that has been measured. The estimated mass
of this one individual plant is 5,900 metric tons, an estimated 59 times
the mass of the honey mushroom fungus or an adult blue whale! Like the
individual honey mushroom fungus, aspen clones can occupy a large area.
Thousands of trunks are part of this one individual organism, and they
occupy over 100 acres. Multiple trunks of a single individual make that
individual more than just the sum of the parts. The parts can cooperate
together to transduce more energy from photosynthesis and better com-
pete for space and light.
Although the trunks in an aspen individual are all connected by their
roots, there may be parts that are not connected physically and yet may be
considered an individual. This possibility was considered with the honey
mushroom fungus. This may stretch someones conception of the indi-
vidual, yet the emergent property that arises is analogous to that which
was discovered for fungi and plants. A part cannot survive by itself, the
individual is greater than the sum of the parts, and parts create properties
that do not exist within the parts. Consider a species of animal where
individuals live together in a colony. Honey bee (Apis mellifera) colonies
have been studied by many researchers. Honey bees and some other
insects can produce heat metabolically; most insects cannot. Anton
Stabentheiner and his colleagues examined body temperatures of honey
bees and temperature regulation of honey bee colonies under varying
temperatures using infrared thermal imaging (Stabentheiner et al., 2010).
The researchers used three experimental hives covered with a plastic
film transparent to infrared radiation. Each hive had a tube connected
to the hive entrance through which bees came and went. Approximately
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 11

150 workers were marked with colored paint that indicated the date and
transferred to experimental hives every other day until colonies contained
4,000 to 5,000 worker bees, which took about 4 weeks. Once a hive was
of a certain age, the queen began producing her own workers, and those
bees were unmarked.
The scientists manipulated temperature by placing hives in a stream
of air at one of five temperatures. The scientists measured air temperature
near bees using thermocouples in various places within the hive, includ-
ing near sealed brood cells (where larvae developed), open brood cells
(where larvae are fed by workers), empty cells, pollen cells (where pollen
is stored), and sealed or open honey cells (where honey is stored).
The scientists measured the head, thorax, and abdomen temperatures
of marked bees of varying ages in different positions in the hive (Figure 3).
The scientists recorded the bees position, its age, its temperature, and the
hive temperature where the bee was located (Figure 4).
The researchers calculated the percentage of bees of each age in
each location at each ambient temperature with thorax temperatures

36, 0C
36

34

32

30

28

26

24

23, 0C

Figure 3 Infrared thermogram of honey bees. On the left and right

are two light gray bees whose thoracic temperatures are ~25o C; on
the top is a bee whose thoracic temperature is 35.6o C, and on the
bottom is a bee whose thoracic temperature is 32.4o C.
Source: Figure 1 from Stabentheiner et al., 2010.
12 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

= Tthorax
= Tcell rim
47
1183
= Ta

436
487
1410
836

234
496

540
370
1079

364
711

345
284
533

270
171
334

56
560

250
temperature (C)

450

63
60
404

387
37

174

74
74

42
27

17
Texp (C)
15
20
25
30
34
15
20
25
30
34
15
20
25
30
34
15
20
25
30
34
15
20
25
30
34
15
20
25
30
34
sealed brood open brood empty cells pollen open honey sealed honey

Figure 4 Thorax temperatures of worker honey bees in different hive

locations at each experimental temperature. Circles and squares
represent median comb cell rim and air temperatures (Ta) at a bees
location, respectively. The thorax temperatures are represented
as a box plot. The center line is the median, the upper and lower
boundaries of each box are the first and third quartile measurements,
and the ends of the bars are the maximum and minimum. Numbers
above each box plot are sample sizes.
Source: Figure 2 from Stabentheiner et al., 2010.

higher than their head and abdomen. Percentages of workers of differ-

ent ages with such thorax temperatures around brood cells are shown
in Figure 5.
When a honey bee hive is stressed by cold temperatures, workers re-
spond by generating heat. At low experimental temperatures, all hive air
and cell rim temperatures were above the experimental temperature, al-
though cells that contained developing larvae and pupae were kept the
warmest. Although there was a wide range of temperatures in worker bees
around the brood, empty, and pollen cells, the median thorax tempera-
tures were higher by several degrees in and around brood cells. As a result,
brood cells were generally kept above 30o C. Cells with honey were not
kept as far above the low experimental temperatures as brood cells were.
At high experimental temperatures worker bee body temperatures were
not that variable and most were close to or only a couple of degrees above
the experimental temperatures.
The generation of body heat is primarily accomplished using large
thoracic flight muscles. Worker bees older than 2 days are much more
likely to be involved in metabolic heat production than bees less than
 THE DEFINITION OF THE INDIVIDUAL CAN BE STRETCHED 13

100 brood

percentage of worker bees

= 0-2d
75 > 2-7d
> 7-12d
> 12d
50

25

0
15 20 25 30 34
A experimental temperature (C)

100 non-brood
percentage of worker bees

75

50

25

0
15 20 25 30 34
B experimental temperature (C)

Figure 5 Percentage of bees with thorax temperatures 0.2o C above

head and 1.0o C above abdomen temperature at five experimental hive
temperatures. A, Bees on brood cells. B, Bees in all other locations
(honey, pollen, and empty cells).
Source: Figure 5b from Stabentheiner et al., 2010.

2 days old. Insect development is temperature dependent. Developing

larvae and pupae cannot produce metabolic heat as worker bees can, and
young workers may not be as good at it as older bees. Workers near the
brood cells are generating more heat than workers in other areas, and
these are primarily older workers. But not all workers are generating heat
at any one time. This indicates division of labor among the members of
the hive. The generation of metabolic heat represents an energetic cost, so
individual bees may be generating heat only for short periods of time and
14 EMERGENT PROPERTIES OF INDIVIDUAL ORGANISMS

taking turns with the task. Additionally, honey bees of different ages ap-
pear to be performing different tasks, which is something that individual
cells in a multicellular organism do.
Although a colony of bees is a collection of individuals, the entire
hive may act like an individual, which is called a superorganism by some
scientists. The hive is a property that emerges from a collection of honey
bees, each a part of the whole, and the properties of the hive are greater
than the sum of the parts. Honey bees produce metabolic heat to main-
tain the temperature of the hive within certain limits but only at or near
brood cells. This is analogous to the maintenance of constant body tem-
perature in an endothermic animal. Thermal homeostasis of a honey bee
colony is the result of the cooperation of thousands of individuals. Our
concept of the individual can be expanded to include biological entities
like a honey bee hive. The study presented here explores but one aspect of
honey bee hives as individuals. In fact, the hive is a highly integrated en-
tity, and bees exhibit communication to more efficiently forage for food,
defend the hive, and grow. The cells and tissues in an individual animal
also display these properties.
Multicellular organisms display division of labor. Within an indi-
vidual organism, a variety of cells perform different tasks, and all of the
cells are integrated into a whole organism. The individual is a property
that emerges from this collection of parts. An individual organism can be
more than that, and the boundary of an individual is not always clear. An
organism may only be part of a much larger whole with the parts com-
municating and cooperating to produce a biological entity that has more
flexible responses to varying environmental conditions than any single
part has.

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 Index
Adrenal glands, 22 Dopamine, 27
Adrenalin, 2123 Dreyer, George, 23
Age appropriate behavior, 26
Airborne mechanism, 32 Emergent property, xiii
Allele, 3, 9 Emotions, 17
Anderson, James, 16 Expressive behaviors, 18
Anger-or-fear response, 22
Anger stimulus, 19 Fear, 18
Armillaria gallica (A. gallica), 12 stimulus, 19
growth rate, estimation of, 5 Fight-or-flight muscle, 22
Atropine, 23 Fungus, 12
Attention deficit hyperactivity growth of, 6
disorder (ADHD), 26
Autonomic nervous system, 24, 25 Growth rate, estimation of, 5
Ax, Albert, 19
Haploid mycelia, 3
Basidiospore, 3 Heart rate, 19
Behavior and Information Heterozygosity
Exchange, 29 in nuclear genetic loci, 4
Behaviors Honey bee (Apis mellifera), 10
age appropriate, 26 infrared thermogram of, 11
emergent property, 25 metabolic heat, production
expressive, 18 of, 14
Brood cells, 1112, 13 thermal homeostasis, 14
thorax temperatures, 12, 13
Cannon, William, 2122 Human brain, xiii
Central nervous system (CNS), 27 Hyphae, 2
Colonies, 33
size, 37 Individual organism, definition
Cooperation, 33 of,114
emergent property, 40
mechanisms of, 29 Karban, Richard, 2930

Darwin, Charles, 29 Lie-detector, 19

The Expression of The Emotions in
Man and Animals, 17, 18
Diastole, 20
Diploid cell, 3
Division of labor, 34
DNA fragments, patterns of, 3
Dominance hierarchy, 34, 35, 40
Mass, estimation of, 5, 10
Mating types, in haploid
mycelia, 3
Methylphenidate, 2728
Microsatellite DNA, 7
Mock, Karen, 710
48 INDEX

Multicellular organisms, 14 Random amplification of

Muscle tension, 19 polymorphic DNA
Mushrooms, 2 (RAPD), 4
wet mass of, 6 and RFLP data, 4
Mutation, 10 Respiration rate, 19
Mycelium, 2 RFLP
and RAPD data, 4
Natural selection, 18, 32 Rhizomorphs, 3
Nervous and endocrine systems,
1728 Sagebrush (Artemisia tridentate),
2930, 40
Paper wasps, 33 Sampling scheme, 7
P. Canadensis, 33, 35, 37 Self-incompatibility
P. fuscatus, 33 of fungi, 3
Physiological response, 19 Skin conductance, 19
changes in, 20 Smooth muscle, 21
Polistes, 33 Stem, genotype of, 78
Polygraph, 19 Subordinate, workers, 34
Polymerase chain reaction (PCR) Superorganism, 14
primers, 4 Systole, 20

Quaking aspen Tibbetts, Elizabeth, 3839

(Populus tremuloides), 7
genetic analysis of, 8 West-Eberhard, Mary Jane, 33, 35
 OTHER TITLES IN OUR BIOLOGY
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Ecological Interactionsby Christopher J. Paradise and A. Malcolm Campbell
Organismal Homeostasisby Christopher J. Paradise and A. Malcolm Campbell
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