Evolution of Interactions in Communities Biology Collection

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FOR THE inCommunities

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Christopher J. Paradise A. Malcolm Campbell
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LIBRARY Pairwise and diffuse coevolution are defined, with examples
that include mutualisms and predator-prey interactions. In any
Create your own example of coevolution, the costs and benefits to both spe-
Customized Content cies involved in the interaction must be assessed in order to
understand evolution of the interaction. Models to explain coral
Evolution of
Bundlethe more
bleaching are examined in the context of a coevolutionary mutu-
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alism, as are the implications for the possible extinction of coral
the greater your
Interactions in
reefs. Data are examined in order to determine which model
discount! is best supported. Other examples of how evolution affects
interactions and communities of organisms include adaptation
THE CONTENT
Energy Physics
to living in particular habitats and evolution to frequent and
somewhat predictable disturbances. For the former, physiologi-
cal adaptations possessed by some plants to live in low light
Communities
Engineering conditions are described and assessed. Ecological disturbances
Biotechnology are defined, and the role of disturbance on evolution of eco-
Biology logical systems is assessed through the use of data. Finally, how
time and spatial scales affect disturbances and the evolutionary
Mathematics
responses of organisms to disturbances are also examined.
Chemistry
Christopher J. Paradiseis professor of biology and environ-
mental studies at Davidson College. He teaches introductory
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A. Malcolm Campbell
Evolution of Interactions
in Communities
Evolution of Interactions
in Communities
Christopher J. Paradise, PhD

A. Malcolm Campbell, PhD
Evolution of Interactions in Communities
Copyright Christopher J. Paradise and A. Malcolm Campbell. 2016.
All rights reserved. No part of this publication may be reproduced, stored

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Abstract
Pairwise and diffuse coevolution are defined, with examples that include
mutualisms and predator-prey interactions. In any example of coevolu-
tion, the costs and benefits to both species involved in the interaction
must be assessed in order to understand evolution of the interaction.
Models to explain coral bleaching are examined in the context of a coevo-
lutionary mutualism, as are the implications for the possible extinction
of coral reefs. Data are examined in order to determine which model is
best supported. Other examples of how evolution affects interactions and
communities of organisms include adaptation to living in particular habi-
tats and evolution to frequent and somewhat predictable disturbances.
For the former, physiological adaptations possessed by some plants to
live in low light conditions are described and assessed. Ecological distur-
bances are defined, and the role of disturbance on evolution of ecological
systems is assessed through the use of data. Finally, how time and spatial
scales affect disturbances and the evolutionary responses of organisms to
disturbances are also examined.
Keywords
ecological systems, habitats, communities, interactions, adaptive evolution,
nonadaptive evolution, natural selection, predators, prey, coevolution,
pairwise coevolution, diffuse coevolution, natural enemy, carnivores,
herbivores, parasites, selective agents, mutualism, pollination, endo-
symbionts, pathogens, coral reef, intraspecific competition, disturbance,
interspecific competition, species distribution, fire ecology
Contents
Preface...................................................................................................ix
Acknowledgments....................................................................................xi
Introduction.........................................................................................xiii
Chapter 1 Species have Evolved as a Consequence of
their Interactions with Other Species.................................1
Coevolutionary Mutualism................................................2
A Predator-Prey Arms Race................................................8
Diffuse Coevolution.........................................................11
Chapter 2 Corals are Bleaching Around the World...........................17
Chapter 3 The Amount of Light Affects the Distribution of
Photosynthesizing Organisms..........................................27
Chapter 4 Organisms in Ecological Communities have Adapted
to Disturbance.................................................................35
Organisms can Adapt to Fire............................................36
Organisms on Rocky Shores are Adapted to Regular
Disturbance..................................................................38
Ethical, Legal, Social Implications: Policy can be used
to Help Prevent Forest Fires..........................................41
Conclusion............................................................................................45
Glossary................................................................................................47
Index....................................................................................................49
Preface
This book about evolution of interactions in ecological communities

is part of a thirty book series that collectively surveys all of the major
themes in biology. Rather than just present information as a collec-
tion 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 con-
text and comprehensive 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 en-
tire discipline: information, 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 evolution of interactions 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 the evolution of interactions the way professional scien-
tists 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 gener-
ous gift of Dr. David Botstein who shared some of his Breakthrough
Prize with co-author AMC. Davids gift allowed us to hire talented art-
ists (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
administrators 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
Terrestrial ecological systems are recognizable most easily by the types

of plants living in them. At the broadest scale of examination, there are
forests, grasslands, deserts, and more. Closer examination of an ecological
system, such as a forest, reveals interesting patterns. Forests exposed to the
same climate conditions have similar types of plants: Forests in Canada
and northern Russia are composed primarily of evergreen trees with needle-
like leaves, whereas forests in more temperate latitudes are composed of
broad-leaved trees. Evergreen forests on two different continents are not
made up of the same species, yet pines, spruces, and firs exist on the
two continents. Habitats separated geographically have similar ecological
conditions and contain species that have similar traits. Entire communi-
ties evolve and adapt to the abiotic conditions to which they are exposed.
Interactions among species in those ecological systems also evolve.
When large scale environmental conditions change, the entire com-
munity must adapt, relocate, or go extinct. Populations evolve through
adaptive and nonadaptive evolution in the context of their environment.
Natural selection leads to adaptations that help species deal with environ-
mental challenges and allow them to obtain resources while minimizing
costs. Species respond uniquely to environmental change, and because
each species responds differently, entirely new communities may arise in a
location undergoing changes in biotic or abiotic conditions.
In this book, which focuses on evolution of multiple populations,
evolution of interacting species, evolution of entire communities, and
evolutionary consequences of rapid environmental changes will be exam-
ined. The main themes of evolution will be evident throughout. Natural
selection is the mechanism that accounts for adaptation to the selective
pressures of interacting species. The evolution of plants that can live on
land led to entirely new communities on the planet, and those commu-
nities are the ancestors of modern day terrestrial plant communities. Life
continues to evolve as the environment changes, and humans are a major
contributor to changes in our twenty-first century environment.
CHAPTER 1
Species have Evolved as

a Consequence of their
Interactions with Other
Species
Animals that use other organisms as resources, or the organisms that are
the resources, act as selective agents on the species with which they inter-
act. A cheetah runs as fast as it does because its prey runs fast. If it could
not run faster than its prey, even for a short time, it would not be able
to catch them. Predators have evolved a variety of strategies for hunting
prey. Prey are under selection pressure to evolve traits that will help them
escape predation. Gazelles, a major prey species of cheetahs, run fast, but
they have also evolved the ability to run in a zigzag pattern and can make
very sharp turns at high speeds. This is something that cheetahs cannot
do as well, and it is a gazelle adaptation for evading the cheetah. The
individuals that possess the traits that best help them escape predation
will be the ones that are most successful in passing those traits on to their
offspring. The trait will then spread through the population. This mecha-
nism of evolution, natural selection, has been explored in other books in
this series, but here the idea of coevolution, which is reciprocal natural
selection of two or more species where each species acts as a selective agent
on at least one other species for traits specific to their interaction, will be
examined in detail.
Often it is clear that particular adaptations have been selected for
by a specific interaction between two species (pairwise coevolution).
Interactions do not always need to be between only two species. Sev-
eral predator species may feed on and act as selective agents on a prey
2 EVOLUTION OF INTERACTIONS IN COMMUNITIES
species, and the prey also selects for certain traits on all of its predators
(diffuse coevolution). Most organisms are resources and are attacked
by more than one natural enemy. For coevolution to occur, a species
must act as a selective agent on another species with which it interacts. A
predator that feeds on several different prey species may have very little
effect on any one species that it eats only rarely. If the prey has acted as
a selective agent in the evolution of the predator but the predator has
not caused evolution of the prey, coevolution has not occurred. On the
other hand, several predators that use the same mode of feeding and
all feed on the same species of prey may act as selective agents in the
evolution of an adaptation that defends against that mode of feeding,
and that anti-predator defense may in turn act as a selective agent in the
evolution of predator adaptations to overcome that defense. That is dif-
fuse coevolution.
Coevolutionary Mutualism
There are many types of interspecies interactions. Natural enemies include
carnivores, herbivores, and parasites. Carnivores are animals that eat ani-
mals. Herbivores are animals that eat plants. Parasites are organisms that
live on or in another organism. Two species may compete for resources
and act as selective agents to each others ability to obtain those resources.
While there are many potential examples of coevolution based on any two
species interactions, for any interaction there must be clear evidence of
reciprocal natural selection of the two species acting as selective agents on
each other in order to conclude that coevolution is occurring.
In another type of interaction, two species may benefit from the pres-
ence of each other, in a mutualism. A mutualism is a relationship between
individuals of different species in which both individuals benefit from
the association. Each of these interactions can lead to pairwise or diffuse
coevolution. The process of pollination is a mutualistic interaction where
coevolution may be occurring or may have occurred in the evolutionary
history of two or more species. The yucca plants are a group of about
50 species of shrubs and small trees in the genus Yucca. They have tough
evergreen, sword-shaped leaves and large clusters of whitish flowers. Yucca
plants have a close relationship with their animal pollinators, the yucca
SPECIES HAVE EVOLVED AS A CONSEQUENCE OF THEIR INTERACTIONS 3
moths. Each species of yucca has a specific relationship with only one or
several yucca moth species, and each species of moth pollinates only one
or several yucca species.
The female yucca moth collects pollen from yucca flowers by dragging
her mouthparts across the pollen-producing anthers, the male structures
of flowers. The moth stores the packet of pollen under her head. The
female then searches for flowers and lays eggs on other flowers, near or
in the ovaries, where seeds will grow once pollination occurs. After she
lays her egg or eggs, the female crawls up the stigma and places a small
amount of pollen from her packet at the top of the stigma. Because each
flower contains many ovaries, and thus potentially many seeds, a single
female may repeat this behavior multiple times on one flower or on one
plant.
After eggs hatch, larvae crawl toward and begin feeding on developing
seeds, often feeding on multiple seeds. Individual plants can abort entire
flowers if they are infested with too many larvae. At the end of feeding,
a larva crawls out of the developing fruit and pupates in the soil. Emer-
gence of adults after pupation coincides with the next flowering season.
Males wait for females by flowers, and when females arrive, mating occurs
and then females collect pollen.
A mutualism must benefit the species involved. Although there
may be more than one yucca or yucca moth involved in a pollinating
interaction, most yucca moths pollinate and lay eggs on only one yucca
plant species. The active pollination that occurs may be an evolved trait
that goes along with the larval seed eating behavior. Yucca moth larvae
eat seeds of the yucca plants, which is a cost to the plant and a ben-
efit to the insect. The larvae eat only developing yucca seeds. The act of
pollination benefits both the plant and the moths offspring, because seed
development is crucial for propagation of both species. There might even
be a benefit to both species when flowers are pollinated by large doses of
pollen. At the same time, there may be costs to the interaction: Too many
larvae could cause a decline in the number of seeds produced by the plant,
and carrying and spreading a lot of pollen could cost the female valuable
energy resources.
Recall how coevolution requires that each species acts as a selective
agent on the other species and each species should possess adaptations
that evolved in response to the close association with the other species.
Addicott and Tyre studied the interaction between yucca and yucca
moths to determine the pollination behavior moths exhibit. They used
the yucca plant Yucca kanabensis and the yucca moth Tegeticula yuccasella.
Each yucca produces from 30 to 150 flowers in the late spring with up to
10% of those flowers maturing into fruit.
When a moth first flies to a yucca flower, it might be expected by any
thoughtful scientist to pollinate the flower first and then lay eggs, because
the act of pollination is so important that neither species can reproduce
without this act. Alternatively, females may lay eggs first if they detect that
pollination has occurred by a prior visit from another female, or if they
did not happen to be transporting pollen at the time of the visit. The first
behavior that moths exhibited in 100% of visits was to lay an egg.
Addicott and Tyre observed subsequent moth behavior on yuccas
to determine how they spent their time and under what conditions
they pollinated flowers. Each visit was tabulated by whether the visit-
ing female moth possessed pollen, which the scientists could see, and
whether the flowers that were visited had been visited previously. Each
visit by a female was termed a behavioral bout. Most of the moths they
observed possessed pollen and 29% of those moths attempted pollina-
tion if they were on previously unvisited flowers, 10% did not attempt
pollination on unvisited flowers. If flowers had previously been visited,
the situation was reversed: 30% of moths did not attempt pollination
while about 18% did. A very low percentage of moths visited flowers
if they did not possess pollen (10%), and most of those went to flow-
ers that had been previously visited. Three percent of moths actually
attempted pollination on visited flowers even though they themselves
did not possess pollen, while 6% also went to previously visited flowers
but did not attempt pollination.
The scientists next determined the relationship between the number of
pollination events and egg-laying events per visit. In every visit to a plant,
moths always laid an egg first. The scientists found that egg laying was
not always followed by pollination, but the probability of pollination was
affected by two factors: whether the moth in question carried pollen, and
whether the flower had been visited previously. In fact, the most common
situation was where a moth laid one egg and did not attempt pollination.
However, there were also many instances of moths laying multiple eggs
and pollinating multiple times. The slope of the relationship between
number of pollination attempts and number of eggs laid was less than
one, suggesting that more eggs were laid than pollinations attempted.
Thus, many moths laid multiple eggs in the same flower. The more
eggs that a female yucca moth laid on a flower, the more likely it became
that she would pollinate that flower and to pollinate multiple times. It
was also more likely that she would pollinate a flower if that flower had
not previously been pollinated. It is likely that females deposit a chemical
on a flower when laying eggs or pollinating that signals to other females
that the flower has been pollinated before. This adaptation would prevent
wasted effort in pollinating already pollinated plants. This ability also
benefits moths without pollen because they can recognize and lay eggs on
flowers that have been pollinated.
Collection of pollen is important in order for moths to bring pollen
to other plants, and Addicott and Tyre determined the conditions under
which moths were likely to collect pollen during a visit to a flower and
what they did after collecting pollen. Moths were twice as likely to collect
pollen during a flower visit if they did not already carry pollen. Addition-
ally, they were highly likely to fly away from the flower if they had just
collected pollen. All moths that collected pollen, 100%, flew away after
collecting pollen. If they had not just collected pollen, there was only
about a 10% chance that they would fly away.
When female moths lay eggs without pollinating, both plants and
moth larvae incur a cost. The cost to larvae occurs if there is egg-laying
by many females each of which fails to pollinate, leading to lower seed
development. Laying an egg first is likely an adaptation that evolved in
moths to ensure that some reproduction occurs. Each moth must lay her
own eggs, and if a flower is not pollinated, no seeds will develop and there
will be no food for the larvae growing in the flower. However, if there are
enough moths or a moth stays on a flower long enough, the probability
of a flower being pollinated increases, benefitting both the plant and the
moth. If many females lay many eggs on one plant, the cost to the off-
spring of a non-pollinating female would be reduced, because another
female might have pollinated the flower. In other species of yucca moth,
females almost always pollinate right after laying their first egg.
Leaving after collecting pollen is an adaptation that has little apparent

benefit for the moth but a large benefit for the plant. Yucca plants have
limited ability to self-pollinate, and pollen from a flower deposited on the
stigma of that flower will not produce seeds. Pollen collecting and leav-
ing behavior of moths evolved because it is advantageous for a moth to
leave after collecting pollen. If she stays and deposits pollen on the same
flower from which it was collected, it will do no good for either the plant
or the moths offspring. The adaptations of these two species evolved to
facilitate the very specific interaction between the yucca moths and the
yucca plants.
If yucca moths stay a long time on a flower, they deposit many eggs
and also add some pollen. Yucca plants produce many flowers, and only
10% or fewer of those flowers mature to fruits. Many of them do not
get pollinated or receive enough pollen for all of the eggs in an indi-
vidual flower. Inside the fruit are many seeds, and each moth larva can
eat multiple seeds. If the total amount of deposited pollen is low, then
neither moths nor the plant benefit. Yucca plants may selectively abort
developing fruits, such that they fall off the plant. That is a cost to the
plant and to the insects feeding in those fruits, but recall that although
the insects provide a pollination service to the plants, they are also eat-
ing the potential offspring of the plants. Producing flowers and maturing
fruits is an energy intensive process, and plants have evolved to minimize
their losses by aborting developing fruits that have few seeds growing in
them. Aborting developing fruits may be an adaptation to reduce the cost
of supporting fruits that have high numbers of larvae and received low
amounts of pollen.
Huth and Pellmyr performed a study on fruit abortion in yuccas to
determine the costs and benefits of this mechanism and how it relates
to the coevolutionary relationship between yuccas and yucca moths.
The biologists studied Y. filamentosa by experimentally manipulating the
quantity of pollen and the genetic composition of pollen applied to flow-
ers to determine the effects of these factors on fruit abortion and reten-
tion. Huth and Pellmyr manipulated flowers on individual yucca plants
by preventing moth pollination and egg laying; they pollinated the flow-
ers themselves. Pollen was added from three different sources in either
small or large quantities. The small quantity was based on the average
amount of pollen received by flowers from 4 to 5 pollinations, and the

large quantity was about 2.5 times greater than the maximum amount of
pollen deposited by a single female. The three sources were pollen from
the individual, pollen from a different plant, and pollen from more than
one different plant.
Any developing yucca moth larvae in aborted fruits will die. A female
moth can increase retention probability of a developing fruit in which
she has laid eggs by providing a large quantity of pollen. In fact, the re-
searchers found that large amounts of pollen led to significantly more
fruit retention, about three times as many fruits on average, regardless
of the source of pollen. If a female laid many eggs on a single flower and
then did not leave much pollen, there would be a high probability of
fruit abortion, leading to selection against female moths that exhibit such
behavior. In this particular experiment, source of pollen did not make a
difference in fruit retention.
The scientists also estimated how these factors affected the total num-
ber of seeds and seedlings produced, because greater reproductive output
would be favored by natural selection. The scientists collected mature
fruits, dissected some of them, and counted the number of seeds per
fruit. Huth and Pellmyr compared pollen sources and small versus large
pollen treatments. They were also able to distinguish between fertile and
infertile seeds, because the former were black and the latter were white.
The researchers randomly selected fertile seeds from each dissected pod,
and measured the mass of each seed. Seeds were planted in small pots to
determine the percentage of seeds from each fruit that germinated. After a
set period of time growing, the plants were harvested and dried to obtain
total plant biomass.
The researchers found that large pollen loads led to higher percent-
age of seeds per fruit, regardless of pollen source, but that germination
frequency was significantly higher when pollen was from another plant
than from the self, by about 60% to 30%. In situations where plants are
self-pollinated, the lower probability of germination will also lead to a
decision by the plant to abort the fruit. Pollen from other plants led to
greater germination frequency and seedling mass than self-produced pol-
len. Seedling mass was a little bit higher in fruits pollinated by non-self
pollen.
Relating these results to the previous studies of moth behavior, moths

possess behavioral adaptations to pollinate more when laying multiple
eggs and to fly away after collecting pollen. These adaptations evolved
in response to natural selection. These behaviors also increase the plants
reproductive output, because they retain developing fruits that contain
many seeds pollinated during pollination events from multiple female
moths. Some of those seeds may be consumed by larvae, but a typical
moth larva eats only several seeds during the larval stages.
The definition of coevolution requires that each species in the inter-
action must cause natural selection to occur in the other in a reciprocal
fashion. In the yucca plant/yucca moth interaction, the moth causes se-
lection for plants that abort developing fruits that received low quanti-
ties of pollen. The yucca plant causes selection for moths that leave after
collecting pollen. There is a disadvantage to moths that stay, because if
they pollinate that flower, few fertile seeds will develop and the plant may
abort the fruit. In the end, the leaving behavior is advantageous for both
the plant and the moth. In addition, many yucca plants have adapted to
the interaction with yucca moths by no longer producing nectar. Yucca
moths do not collect nectar, and the lack of nectar acts to exclude other
potential pollinators, and this facilitates and strengthens the coevolution-
ary pairwise interaction.
A Predator-Prey Arms Race

Another class of coevolutionary interactions occurs between predators
and their prey and pathogens and their hosts. This kind of coevolution
has been likened to an arms race between nations. The cheetah and gazelle
interaction would be an example of an evolutionary arms race. The arms
race could be pairwise or diffuse and involves the evolution of adapta-
tions to capture prey and anti-predator defenses. The skin of some newts,
a type of salamander, contains tetrodotoxin, which is a potent neurotoxin
that inhibits the propagation of action potentials. Tetrodotoxin is a very
effective defense and can kill predators even in small doses if they have
no resistance to the toxin. The garter snake Thamnophis sirtalis preys on
the rough-skinned newt Taricha granulosa. Becky Williams and her col-
leagues studied the garter snake/rough-skinned newt interaction and the
arms race characterized by the evolution of tetrodotoxin and resistance to

tetrodotoxin.
Individual rough-skinned newts contain variable amounts of tetro-
dotoxin. Of the predators that have been observed to attack these newts,
only garter snakes are known to be resistant to tetrodotoxin. As newts are
variable in tetrodotoxin, so are individual garter snakes variable in resis-
tance to tetrodotoxin. Given the variability in both populations, natural
selection and coevolution could strengthen the interaction. There might
be selection for resistance to tetrodotoxin in populations of snakes living
in areas with newt populations that have high levels of tetrodotoxin. It
might be predicted that resistance to tetrodotoxin in snakes would be cor-
related with levels of tetrodotoxin in newts. Williams and her colleagues
in fact predicted that snakes with higher resistance would be able to con-
sume a toxic newt and survive the encounter.
Williams and her colleagues studied snakes born in captivity that
had no prior experience with rough-skinned newts. Snakes were ex-
posed to newts from a population whose individuals contained more
tetrodotoxin than newts from the area where the captive snakes were
from. The captive snakes not only had never experienced newts, but
they should also have fairly low resistance to more toxic newts, given
that their parents were from a population that typically encountered
low toxicity newts.
The scientists measured resistance to tetrodotoxin by repeatedly
measuring speed of movement before and after injecting snakes with te-
trodotoxin. Resistance was quantified by the post-injection speed as a
percentage of pre-injection speed. Snakes with low resistance had a low
percentage, and those unaffected by tetrodotoxin moved at 100% of their
pre-injection speed. Resistance to tetrodotoxin was then correlated with
how the snakes dealt with newts in encounters with newts (Figure 1A).
The researchers recorded the behavioral interactions between preda-
tor and prey, including whether the newt was captured, released or
swallowed, how long the snake held onto the newt before releasing or
swallowing and whether the newt survived the encounter. Six snakes con-
sumed their newt, but only four snakes survived that encounter. Of the
other fourteen snakes, thirteen rejected their newt, and one did not even
try to capture its prey. All of the rejected newts survived their attack. The
= exposure time
100 180 = recovery time
percent resistance (+ 1 SE)
160
80 140
time (min + 1 SE)

120
60
100
80
40
60
20 40
20
0 0
consumed/ consumed/ rejected/ consumed rejected
lived died lived newt outcome
A newt and snake outcome B
Figure 1 Responses of garter snakes to newts. A, Percent resistance

in snakes that consumed newts and lived or died and in snakes that
rejected newts. Resistance is as defined in text. B, Time that snakes
were exposed to (held in mouth prior to swallowing or rejecting) and
time it took for snakes to recover after encounter with newts.
Source: Data from Williams et al., 2003, Table 1.
percent resistance to tetrodotoxin was related to the categories of how the

snakes dealt with newts (Figure 1A).
One other measure made was time to recover from the effects of te-
trodotoxin exposure. This was determined by how long it took for the
snake to be able to turn on to its belly after being turned on its back by
the researchers. If the snake could not right itself, then it was suffering
from the toxic effects of tetrodotoxin. This was repeated every 5 minutes
to determine recovery time (see Figure 1B).
For snakes that survived encounters, there were differences in how
long the snakes were exposed to the toxin and how long it took snakes
to recover from the toxic exposure (see Figure 1B). All of the snakes,
whether successfully swallowing the newt or not, had difficulty righting
themselves for a period of time and also experienced other symptoms of
poisoning. They writhed around, had difficulty holding their heads up,
and rubbed their open mouths on the bottom of their cages.
All of the snakes were exposed to newts from a population that had,
on average, much higher levels of tetrodotoxin than newts from the area
from which the snakes came. If snakes were exposed to newts from their
home population, they should have been able to handle most if not all
newts. Even when exposed to newts from a population with generally

higher levels of tetrodotoxin, some garter snakes ought to be able to re-
sist those higher levels, and some of those newts may have below aver-
age levels of tetrodotoxin. Williams and colleagues showed that garter
snakes with higher resistance could handle a much longer exposure to
toxic newts and could survive after eating a newt. For snakes that both
consumed and rejected newts, recovery time seemed to be a function of
exposure time. The longer a snake was exposed to a newt, the longer it
took to recover from the exposure to tetrodotoxin.
Snakes that consumed a newt and did not survive had lower resis-
tance than snakes that consumed a newt and survived. This would lead
to natural selection against snakes with lower resistance. Snakes that
consumed a newt and survived may still be selected against if a lower
level of resistance causes them to recover more slowly, leaving them
open to predation by another predator. Again, this leads to evolution
of higher resistance. Differences in resistance have consequences on the
number of offspring that a snake leaves behind. Had those snakes that
died while consuming a newt encountered a newt with a lower level of
tetrodotoxin, they might have survived; and if they had encountered
a newt with higher levels of tetrodotoxin, they might have quickly re-
jected it.
All of the newts that were rejected, even if they were held in the
mouth for many minutes, survived. This means that there is selection for
newts with higher levels of tetrodotoxin. Newts with high levels of tetro-
dotoxin would be more likely to exceed the resistance level of a snake,
thus increasing the newts probability of surviving an attack. Newts with
low levels of tetrodotoxin suffer higher predation by garter snakes, such
that low levels are selected against over evolutionary time. This illustrates
pairwise reciprocal coevolution.
Diffuse Coevolution
One mutualistic and one antagonistic interaction have been examined
that both show pairwise coevolution. Another mutualism that may have
been strengthened through coevolution is that between fruit-bearing
plants and fruit-eating birds that disperse seeds. Plants do not produce
fruits all year long, and many birds consume different fruits at differ-
ent times of the year. Herrera studied a community of fruit-producing
trees and their bird dispersers in Spain. He hypothesized that the propor-
tions of carbohydrates, lipids, proteins, water, and minerals vary in fruits
produced at different times of the year due to coevolution among the
birds dispersing the fruits and the plants producing them. For instance,
there should be more energy-rich lipids in fruits available in the winter.
Herrera conducted his study in forests that have both a dry and a wet
season. He recorded all of the plants that had bird-dispersed fruit in each
study site, which was between 17 and 25 species. For each species, Her-
rera determined the time of year that fruits ripened, using his own obser-
vations and published observations. He then classified each species into
one of three seasonal categories based on when most ripe fruits occurred:
summer, autumn, or winter.
Herrera recorded various characteristics of ripe fruits determined
from a sample of fruits collected from each plant species. The characteris-
tics included the fruit wet mass, fruit dry mass, the percent water content
of the fruit pulp (everything but the seeds), and the number of seeds per
fruit. He then separated out the pulp and determined the average mass
of lipid and protein in the fruits. Herrera pooled the results of all species
present in a season and forest, because his objective was to compare the
fruit features present in different seasons. He also calculated an overall
profitability (OP) measure of the different fruits available in each season.
This net profitability provides a measurable value of costs and benefits
based on the fruit characteristics he measured. The equation he used for
OP in substance i, either lipid or protein, was
OPi 5
(1 2 WP ) * P d
i
P 1S
where WP equals the percent water content of the pulp, P is the total mass
of the pulp, S is the mass of the seeds, and di is the percent mass of pulp
that is made up of substance i.
Notice that there are two main parts to the OP equation:
(12 WP ) * P
P 1S
and di. The first part is a fraction. The denominator is the pulp mass plus
seed mass, so it is just the total mass of the fruit. Because WP is the
proportion of the fruit pulp that is water, 1 WP is the proportion of

the fruit pulp that is not water. Multiplying this proportion by P, the
wet mass of the pulp, gives the non-water mass, or dry mass, of the pulp.
Therefore, the fraction (12 WP ) * P is the dry mass of the pulp divided
P 1S
by the total mass of the fruit. Herrera called this fraction the relative yield,
because the dry mass of the pulp is where all of the nutrition is for the
birds. The greater the pulp dry mass, the greater the profitability of the
fruit.
The most complicated looking part of the OP equation is just the
proportion of the total fruit that provides nutrition to the birds, which
is a number that can theoretically range from 0 (if the fruit were all
water [i.e., WP = 1]) to 1 (if the fruit contained no water and no seeds
[i.e., WP = 0 and S = 0]). The proportion decreases as either water con-
tent or seed mass increases.
While pulp dry mass did not vary across the seasons due to the high
level of variation among the fruits within a season, it did increase on aver-
age from 52.9 ( 56.7 SD) in summer to 97.2 ( 86.9 SD) in autumn
to 122.8 mg ( 245.6 SD) in winter. Fruit wet mass also increased but
not significantly from 324.1 ( 340.6 SD) to 414.9 ( 296.7 SD) to
468.0 ( 738.8 SD) across the seasons. While those variables did not
significantly change across season, Herrera found that percentage water
declined from 67.9 ( 9.3 SD) to 60.0 ( 9.2 SD) to 52.0 ( 16.4 SD)
from summer to winter.
The second main part of the OP equation, di, is the proportion of
the dry mass of pulp that is made up of lipids (i = 1) or protein (i = 2).
Multiplying the relative yield by d1 gives the proportion of the total mass
of the fruit that is lipids; multiplying the relative yield by d2 gives the pro-
portion of the total mass of the fruit that is protein. OP is a very intuitive
measure of productivity: the proportion of the fruit that is a particular
nutritious substance.
When comparing lipid to protein profitability, Herrera found that
both increased significantly from summer through autumn to winter.
Lipid profitability, which includes the percentage content of lipids, but
also the other variables of seed, pulp, and water content in the equation
above, was 0.38 ( 0.21 SD) in summer, 1.55 ( 2.96 SD) in autumn,
and 4.73 ( 4.64 SD) in winter. Protein profitability was 0.69 ( 0.29
SD) in summer, 0.85 ( 0.34 SD) in autumn, and 1.12 ( 0.38 SD) in
winter.
Some of the quantities that Herrera measured were highly variable,
and he found no statistically significant differences in the two mass mea-
surements despite large differences in the mean pulp dry mass from sum-
mer to winter. Although there were differences in the mean masses of
pulp and whole fruits across seasons, there was so much variation around
those means that Herrera did not find significant differences across sea-
son. This could be in part because he pooled all plants ripening fruits
within one season. The high level of variability in mass measurements
might simply be caused by differences among fruit trees. This makes the
more consistent and statistically different means in percent water con-
tent all the more striking.
Plants that produce fruit only do so at certain times of the year, and
in the forests that Herrera studied, fruits were available all year, but the
type of fruit available and its nutritional content varied with the season.
Animals living in a temperate environment with distinct wet/dry or
warm/cold seasons have energy and nutrient demands that also change
over time. Making fruits attractive to bird dispersers by matching fruit
characteristics to bird requirements is important to the plant to complete
its life cycle. Species of plants may have evolved to produce fruits that
contain what the birds need at that time of year.
Herrera found that in the summer fruit consumption and seed dis-
persal was performed by juveniles and non-migrating species that had
mated in the spring. Most fruit-eating birds also consume insects when
they are available. Although protein requirements are high for grow-
ing birds, the abundance of insects in the summer probably reduces se-
lection for fruits with high protein content. In the dry summer, water
availability is more important, and the percentage of water in summer
fruits is significantly higher than in autumn and winter fruits. Filling
fruits with water is costly to the plants, but the benefit of having seeds
dispersed must outweigh that cost. There is a benefit to the birds in
selecting fruits with high water content during the dry season. Several
bird species acting similarly could cause selection for individual plants
that produce fruits with higher water content. Likewise, plant species
producing fruits with high amounts of water in the dry summer would
select for birds that chose those particular fruits to eat. This is diffuse
reciprocal coevolution.
As autumn progresses, temperatures decline, and there is a greater
need for energy in birds to maintain high body temperatures and high
metabolic rates. Lipid content and lipid profitability both increase dra-
matically from summer to autumn to winter. Plant species that ripen
fruits in winter produce fruits with much higher lipid contents than
plants that ripen fruits in the summer. This is a large cost to plants, but
there is clearly a benefit and strong selection by birds for fruits that have
high lipid content. If plants produced low lipid fruits during this time of
year, they would not get their fruits dispersed, leading to selection against
plants with low lipid fruits. Likewise, plants that produce high lipid fruits
will cause selection for birds that eat those fruits. Those fruits will provide
a higher probability of survival of birds in winter, and over time, birds will
evolve to prefer those fruits.
Each plant species has evolved to be attractive to the fruit-eating
birds in their habitat, and they may compete with each other for the
birds to consume their fruits. There is a distinct community of fruit-
producing plants in each season with a somewhat variable community
of birds feeding on those fruits in each season. Because there are several
plants and several birds involved in this interaction, it is an example of
diffuse coevolution. The birds and their needs would add selection pres-
sure such that the birds, as a group, would cause selection for fruits with
the characteristics that best match their nutritional requirements. Plants
that evolved to provide birds what they need in each season would cause
selection for birds that sought out and ate those particular fruits more
often than plant species that produced fruits with less than or none of
the required nutrient. The power of diffuse coevolution is such that
it could affect an entire ecological systemas it appears to have done
here. Other phenomena can affect entire ecological systems, including
ones that have potential negative consequences to those systems and the
species living within them. Such a major event, coral bleaching, will be
examined in the next chapter.
Bibliography
Addicott JF, Tyre AJ: Cheating in an obligate mutualism: how often do
yucca moths benefit yuccas? Oikos 72:382394, 1995.
Herrera CM: Seasonal variation in the quality of fruits and diffuse co-
evolution between plants and avian dispersers, Ecology 63:773785,
1982.
Huth CJ, Pellmyr O: Pollen-mediated selective abortion in yuccas and
its consequences for the plant-pollinator mutualism, Ecology 81:
11001107, 2000.
Iwao K, Rausher MD: Evolution of plant resistance to multiple herbi-
vores: quantifying diffuse coevolution, Am Nat 149:316335, 1997.
Pellmyr O: Yuccas, yucca moths, and coevolution: a review, Ann Missouri
Bot Gard 90:3555, 2003.
CHAPTER 2
Corals are Bleaching

Around the World
The expression, use it or lose it, is very common and most people are
probably familiar with it. Many people that learned a foreign language
might lose their ability to speak if it they do not use it, or lose skills in
a sport or a musical instrument that they no longer play. Professionals
make their skills look easy, but even the worlds best golf player practices
putting every day. It might seem strange, but a modified version of the
expression, use it or lose it, holds for cells and organisms, toounused
genes will be lost over time, and there are many examples of organisms
with relatively small genomes (Table 1). In this section, coral reefs will
be examined, which are structures largely built by coral animals, many of
which harbor symbiotic photosynthetic dinoflagellates, a type of algae.
The organisms and their genomes are being challenged. The challenge
is global climate change, and the likelihood that the two genomes in
coral will be able to evolve fast enough to survive or go extinct will be
examined.
Compared to a typical bacterium, such as E. coli, the species listed in
Table 1 have small genomes that encode very few proteins. Only one of
these microbes is an Archaean, but all of them are either endosymbionts,
organisms that live inside the cells of other species, or pathogens, disease-
causing organisms. These species are dependent upon their host species to
supply them with energy and other metabolic products. Pathogens harm
their hosts, but some endosymbionts pay metabolic rent to their hosts in
exchange for reliable room and board. Because their hosts supply criti-
cal metabolites to the microbes, the microbes experience selection pres-
sure to reduce their burden and get rid of genomic excess baggage. Large
genetic changes can occur quickly and can produce variation within a
Table 1 Microbes with small genomes, compared to E. coli.

species domain description genome Mbps proteins
Candidatus Carsonella ruddii bacteria plant-eating insect endosymbiont 0.16 182
Candidatus Sulcia muelleri bacteria a leafhopper symbiont 0.25 227
Buchnera aphidicola bacteria endosymbiont of the aphid 0.42 362
Nanoarchaeum equitans archaea hot vent tube worms symbiont 0.49 536
Mycoplasma genitalium bacteria urinary tract pathogen 0.58 477
Candidatus Phytoplasm mali bacteria apple proliferation disease 0.60 479
Ureaplasma parvum bacteria urinary tract pathogen 0.75 614
Mycoplasma pneumoniae bacteria bronchitis and pneumonia 0.82 689
Borrelia turicatae bacteria tick-borne relapsing fever 0.92 818
leads to blindness and sexually
Chlamydia trachomatis bacteria 1.00 874
transmitted diseases (STDs)
Escherichia coli bacteria diarrhea (from undercooked meat) 5.50 5,423
Source: From http://www.ncbi.nlm.nih. gov/genomes/lproks.cgi
population. If a microbe deleted a gene that it no longer needed, then

the reduced genome could provide a selective advantage. Over millennia,
pathogens and endosymbionts have lost genes that they dont need and
their genomes get smaller.
Endosymbionts are absolutely vital to the health of our planet. In
fact, the largest living coral reef system in the worldthe Great Barrier
Reef of Australiabenefits from endosymbionts. Coral reefs are colonies
of many tiny animals with endosymbiotic photosynthesizing organisms
living inside the animal cells. Coral animals have a complex life cycle
that involves two stages, free-swimming and stationary. New individuals
are formed when sperm and eggs fuse to produce larvae that float in the
water. Soon, the larvae swim until they find suitable places to settle and
change shape to match their new lifestyle. The new shape is similar to a
hydra in that it has a short trunk that terminates in a mouth surrounded
by tentacles. However, what may not be commonly known is that coral
benefit from photosynthetic algae that they acquire for the first time dur-
ing the larval stage in a mutualism.
Coral are not born with their symbiotic algae. Coral larvae eat the
algae, some of which move from the digestive system to inside animal
cells of their new hosts. The algae supply their animal hosts with energy
derived from photosynthesis. The coral animal captures microscopic prey
with their tentacles, and they share the consumed nutrients with their
symbiotic algae. Algae are unicellular photosynthesizers that capture sun-
light for energy and contain a range of different pigments that provide
them with the many different colors that are observed in coral reefs. The
Corals are Bleaching Around the World 19
photosynthetic pigment called chlorophyll fluoresces red when stimulated

by UV light.
In Table 1, it was shown that endosymbionts tend to have small ge-
nomes, perhaps after becoming dependent upon larger hosts that sup-
ply them with needed metabolites. Endosymbionts are cells living inside
other cells with each species evolving a dependence on the other for
some of their nutrients or energy. Beginning in 1987, marine biologists
recognized a new pathology in coral reefs in the Caribbean Sea that re-
sulted in a loss of endosymbionts. For an unknown reason, big patches
of colorful coral reefs were turning white, as if they had been bleached.
This bleaching disease was most common in the months of August,
September, and October. Approximately 70% of total reports of bleaching
occurred in those months, according to McWilliams et al. (2005). Less
than 10% of bleaching events occurred between December and April.
Because reefs are the foundation for entire ecosystems that support a
large proportion of the worlds fish, losing coral could be a global disaster.
It was important for marine biologists to figure out why the coral was
bleaching.
The coral and algae species coevolved to benefit from each other, so
it stands to reason that bleached coral must be suffering from the lack of
metabolic support they used to receive from their endosymbionts. Given
that the hottest months in Caribbean Islands, such as the Bahamas, are
June to September, it is not surprising to find out that bleaching has a
positive correlation with the temperature. Therefore, it is reasonable to
hypothesize that the bleaching is related to elevated water temperatures,
but data are needed to support or reject this hypothesis.
To determine if water temperature influenced coral bleaching, five
ecologists, McWilliams and colleagues, from Norwich, UK, compared
observations of bleaching and water temperatures, using the measure of
variations from a long-term average temperature. For the 18 years ana-
lyzed, bleaching in the Caribbean was at its worst in 1998, which also
was the hottest summer on record at that time. However, no one has
devised a standardized way to quantify bleaching, so the available data
were collected from published reports that used qualitative terms, such as
massive, severe, and widespread. Due to the non-standardized data,
it was very difficult to quantify the data.
However, McWilliams and his colleagues found that the log-

transformed number of 1 latitude by longitudinal cells in the Caribbean
Sea was positively related to sea surface temperature (the regression equa-
tion was log[cells] = 1.34[SST] + 0.71). This relationship was found for
events between 1983 and 2000 (r2 of 0.86; P < 0.001). For the same time
frame, the researchers counted how much ocean surface area had at least
one report of bleaching. They found that the total area of the Caribbean
was positively related to sea surface temperature as well. That is, as tem-
peratures increased, so did the extent of coral bleaching events (regression
equation was [area] = 3784[SST] + 909; r2 = 0.72; P = 0.001).
The relationship between sea surface temperatures and the extent of
bleaching is linear, but that is based on log-transformation of the number
of map grid cells or area of bleaching. Therefore, the percentages increase
exponentially as the temperature variation increases. An increase of 0.1 C
corresponds to larger and larger increases in the percentage of regions
with bleached coral. The largest percentage in this study was about 45%,
so scientists must extrapolate far outside of the data to predict the tem-
perature variation at which the percentage is at least 95%. Extrapolation
is the application of a mathematical model outside of the range of data
that were used to build the model equation. The data indicate that a
variation of 0.72 C leads to just 101.63 = 43% bleaching. However, a
variation of 1 C is predicted to produce approximately 100% bleaching.
Unfortunately, such outcomes cannot be predicted with great certainty
until a more extreme event occurs, and then it might be too late.
If increased water temperature causes bleaching, then bleaching may
be a world-wide phenomenon (Figure 2). All over the world, reefs are suf-
fering from bleaching, and the bleaching correlates positively with water
temperatures. The degree of bleaching varies around the world, but keep
in mind that no one has developed a quantitative, standardized method
to measure bleaching, there is variation in ocean temperatures, and the
oceans are not heating up evenly.
Many biologists are collaborating to determine the mechanism that
causes bleaching. When coral bleaches, it can lose as much as 90% of its
algae, and the remaining algae lose about 90% of their photosynthetic
pigments, leaving coral with 1% of their original photosynthetic capacity.
After the coral animals living at the extremities of the reef structure lose
B
= high
= medium
= low
= no bleaching
= severity unknown
Figure 2 Global coral bleaching in 2007. A, Qualitative data from

around the world showing the degree of coral bleaching. B, Zoomed in
view of Caribbean and Bermuda data.
Source: Screen shots from Reefbase http://www.reefbase.org/global_database
their color, what remains is the white, calcium-rich exoskeleton of the

coral, which is the reef structure.
Currently, biologists have proposed two mechanisms to explain why
most of the algae are gone. One mechanism could be called the bad
tenant model, which proposes that the algae do not function well in
the warm water and their productivity is reduced. As a result, the algae
provide the coral with fewer metabolic benefits, and so the coral animals
expel the algae into the open ocean. Conversely, the crummy landlord
model proposes that the coral animals are stressed by the heat, and they
fail to support the algae adequately. As a result, the algae produce toxic
compounds, and this causes the coral animals to expel the algae in self-
defense. Regardless of the mechanism, coral animals are left to fend for
themselves and cannot survive long without its mutualistic algal partner,
because coral has evolved to become dependent upon their intracellular
symbionts. Remember that endosymbiotic genomes tend to get rid of

genes that their symbiotic partners supply. When temperatures cool
down, many coral animals can recover their endosymbionts and survive,
but if bleaching is lengthy or recurrent, coral animals will not survive.
Possessing mutualistic algae is the product of natural selection: vari
ation among individuals, overproduction of offspring, limited resources,
intraspecific competition, selective advantage, and reproduction. As the
oceans continue to warm, the selection pressure on all species is shifting
so that only heat tolerant coral animals and algae can persist. For coral
animals, a slight increase in water temperature is one cause of bleaching
that has been replicated under laboratory conditions. Human behavior is
contributing to global climate change, which means humans are affecting
coral evolution.
Global temperatures fluctuate from year to year, but on average the
temperature is climbing and the rate of increase has been increasing in
recent decades. Marine biologists are trying to understand the future
implications of global climate change. They have developed three theo-
retical models of coral evolution. In the fixed threshold model, which is
consistent with regression equations of bleaching extent and sea surface
temperatures, a fixed temperature threshold induces coral bleaching. The
fixed threshold model means extinction of coral is certain as global tem-
peratures rise.
The graded threshold model suggests different temperatures might in-
duce bleaching differentially for various coral and algal species. Because
there are many species of coral animals and many species of endosymbi-
otic algae, it seems unlikely that all coral will die at the same tempera-
ture threshold. Graded threshold is consistent with the observation that
bleaching happens in blotchy patches and not uniformly in a region,
which is also consistent with the regression equations discussed above.
One coral colony may be pure white, whereas its neighbor looks color-
ful. Therefore, depending on the different heat tolerance of the mutualis-
tic coral and algae, bleaching probably happens at different temperature
thresholds for different species.
The most complex, but perhaps most realistic model, is the evolv-
ing threshold model, which suggests threshold temperatures increase over
time. The threshold increases because the coral and algae are evolving
over time to become more heat tolerant. The evolving threshold model
means that the survival of coral depends upon whether evolution of coral
animals and their symbionts can keep pace with global climate change.
Genomes can change very quickly if selection pressures are strong. If evo-
lution can keep pace, coral reefs might survive into the twenty-second
century.
If the fixed temperature threshold is true, then different species of
algae should have the same responses to elevated temperatures. Biologists
at the Guam Marine Laboratory experimentally tested the temperature
sensitivity of two algae living in a single coral species (Table 2). As in-
dicated by the asterisks, photosynthesis for one species was significantly
greater at 31.3 C and 32 C compared to 28.5 C. The other alga species
had a significantly reduced photosynthetic capacity at 32 C compared
to 28.5 C. Furthermore, the two algae were significantly different from
each other at both 31.3 C and 32 C. The data refute the fixed threshold
model, but there is not have enough data yet to reject the graded or evolv-
ing threshold models.
Change in allele frequency over time is evolution; so algae might
evolve different thermal tolerances over time, but how fast? Through
evolution, we would expect heat-tolerant algae to become more abun-
dant in each ecosystem and thus bleaching should be reduced over time
if the warming is slow enough. The benefits of heat tolerance may lead
to fewer coral animal species that can accept the heat-resistant algae, and
thus some coral species may become extinct while others thrive. If the
coral and algae coevolve, the modified mutualism may affect reproduc-
tive success and thus the number of individuals surviving in subsequent
generations. But it is impossible to model the future with certainty when
information is incomplete.
Evolution does not occur at a constant rate. Populations can change
rapidly in short time periods. However, due to the random nature of the
variation within populations, we cannot predict whether heat tolerance will
evolve quickly or slowly. If the rate of global climate change exceeds the rate
of evolution, coral animals will go extinct, and their symbiotic algae will
too. The loss of reefs would further accelerate the increase in atmospheric
carbon dioxide (CO2), because the algae will have stopped photosynthesiz-
ing. Furthermore, the loss of coral reefs would likely lead to the extinction
Table 2 Comparison of two species of algae and their relative capacity

to photosynthesize (1/2 1 SD). indicates significant differences
(p , 0.05) between the elevated and baseline temperatures for species 2;
* indicates significant differences (p , 0.05) between the elevated
and baseline temperatures for species 2; and indicate significant
differences (p , 0.05) between species at a given temperature.
algal relative photosynthestic differences within differences
temperature (C)
species capacity a species between species
1 0.540 0.021
28.5
2 0.568 0.029
1 0.543 0.030
31.3
2 0.619 0.023 *
1 0.469 0.032
32.0
2 0.617 0.024 *
Source: From Rowan, 2004, Figure 1a.
of many marine organisms, which would severely impact human food sup-
plies. In short, if coral animals and symbiotic algae evolution cannot keep
pace with the rate of ocean warming, then the world will face a catastrophic
ecological collapse. If algae cells produce large genome changes quickly, the
population may contain enough variation to slow bleaching, survive ocean
warming, and prevent a global food shortage for humans.
While it is not known for certain how coral animals and their symbi-
otic algae will respond, some biologists have already demonstrated what
can be done to slow coral bleaching. Marine protected areas can be used
to nurture heat-tolerant symbiotic coral and algae. These reefs can serve
as genetic repositories that can be used to recolonize coral reefs affected
by bleaching. There is clear evidence that algae recolonization will work
based on data after the 1998 extreme bleaching. Coral reefs that recovered
the fastest were downstream of prevailing water currents that carried heat
resistant larvae from healthy reefs.
Beyond 2000, sea surface temperatures have continued to be high.
Temperatures in 2005 were hotter even than measured in the earlier study,
and even more coral bleaching was reported. Coral grows where tempera-
tures average between 28 C and 32 C. Ocean currents circulate to bring
warmer or colder water to an area. Water off the US West Coast comes
down from the Arctic and is colder than the water off the East Coast of
the US, which comes up from the tropics. As ocean temperatures warm,
coral may migrate toward the cooler water near the poles. The coral reefs
cannot migrate, but coral larvae can float on ocean currents and settle in
cooler water. If coral does migrate with the ocean currents, coral off the
US Atlantic Coast could move north to cooler waters, whereas Pacific
currents would lead to unfavorable movement to warmer waters.
This chapter addressed mutualistic endosymbiosis and coevolution of
algae and coral animals. Variant cells within the natural population might
be better adapted than others to the warming oceans. Temperature cannot
be the only variable related to coral bleaching. Reefs with no bleaching
are known to be right next to areas of severe bleaching. This non-uniform
distribution indicates that genomic factors probably also play a role in
coral bleaching. Gene flow, horizontal gene transfer, mutations, and natu-
ral selection could all play a role in the evolution of coral animals and
their endosymbiotic algae. The time scale of this evolution and the rate of
global warming cannot be measured in advance, so this experiment will
unfold in the next few decades.
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CHAPTER 3
The Amount of Light

Affects the Distribution
of Photosynthesizing
Organisms
Evolutionary processes can be better understood by exploring how a

group of species with different adaptations is distributed within a habitat
with variable conditions. Consider the amount of light in a forest or a
lake. When light strikes the surface of the water or the top of the tallest
trees in a forest on a sunny day, the light is at its brightest. The amount
of light that penetrates deeper into a forest or lake decreases steadily, and
its spectral quality changes. For a plant in the forest or an algal cell in
the lake, individuals or populations might benefit from living higher up
or closer to the surface, respectively. Species that live closer to the forest
floor might be at a disadvantage, because they do not get enough light.
However, there are costs associated with growing very large or living high
up in the air, and species living close to the ground may have adaptations
that allow them to survive in low light conditions.
Different plant species have adapted to survive in high or low light
and may have even adapted to highly variable light, because plants that
live in the forest may be exposed to alternately dark and light conditions.
When a tree falls or strong winds blow, gaps open that let more light onto
the forest floor. Small plants, like shrubs and short trees, living on the for-
est floor are adapted to these dynamic conditions and might even depend
upon light coming in through gaps.
Robert Pearcy and his colleagues examined photosynthesis in several
species of rainforest shrubs under changing light conditions in three places:
(moles of photons/m2 1 SD) 20 100
intensity periods ( 1 SD)

cummulative daily light
% received during high

16 80
12 60
8 40
4 20
0 0
A understory edge/ clearings B understory edge/ clearings
small gap small gap
140 5000
duration of high intensity
periods (seconds 1 SD)
number of high intensity
periods (# / day 1 SD)
120
4000
100
80 3000
60 2000
40
1000
20
0 0
C understory edge/ clearings D understory edge/ clearings
small gap small gap
Figure 3 Properties of the light environment in the forest understory

near edges or small gaps and in clearings in a Panama rainforest.
A, Average total daily light photons, which is a quantitative measure of
light intensity. B, Percentage of total light from A that was attributed
to light flashes. C, Number of time periods that receive high light
intensity, correlated with number of light flashes. D, Duration of high
light intensity periods, a measure of the length of light flashes.
Source: From Valladares et al., 1997, Table 1.
in the forest understory beneath the tree canopy, along the edges of forests,
and in gaps. The researchers performed their study in a tropical rainforest.
They used photosensors to record light availability over a long period of
time in each habitat type. The total number of photons of light striking a
photosensor was used as a measurement of light quantity. Photons strike
the sensor even when it is shaded, but more photons strike it when exposed
to full sunlight, even if for only a brief period of time. Pearcy and his col-
leagues found that the frequency of bright light periods and the overall
intensity of light varied among the three habitats (Figure 3).
The scientists measured the cumulative amount of light in each habi-
tat (Figure 3A), and from that they determined the percentage of light
THE AMOUNT OF LIGHT AFFECTS PLANT DISTRIBUTIONS 29
that was due to bright periods (Figure 3B). They determined how many
bright, unshaded periods occurred per day (Figure 3C) and the average
length of those periods (Figure 3D). Clearings, for instance, had more cu-
mulative light but fewer bright periods per day. Those periods were much
longer than in other habitats, leading to most of the light in that habitat
coming from long periods of bright, unshaded light.
Plants are adapted to different light regimes. The amount of light and
the pattern of occurrence of high and low light affect the distribution of
these photosynthesizing organisms. Clearings had the highest total light
occurring on a daily basismore than twice as much as edges, and more
than 30 times that of the understory. The latter two habitats had high
frequencies of short duration periods of high intensity light. Plants living
in these habitats were predicted by the researchers to be dependent upon
these short flashes of light, and they adapted to take maximum advantage
of these short duration flashes. The scientists hypothesized that the shad-
ier the habitat, the more dependent plants would be on occasional flashes
(short bursts) of light that passed through the forest canopy.
Three of the species that Pearcy and his colleagues studied were plants
that typically grow in the forest understorytwo were shrubs found
along the forest edge, and the sixth one grows in open clearings. The
scientists used a special chamber in which they could enclose individual
leaves of a plant to measure the flow of CO2 into or out of the leaf under
different light conditions.
The changing CO2 concentration in the chamber reflected the flow
of CO2 between the atmosphere and the plant. During periods of intense
photosynthesis, CO2 concentrations in the chamber dropped, and dur-
ing periods of darkness or low light, CO2 would increase. For each spe-
cies, the researchers determined the maximum net photosynthetic rate,
which is the rate of CO2 used during photosynthesis minus the rate of
CO2 given off during respiration. This is determined by the maximum
amount of CO2 captured by photosynthesis; the light brightness that
causes the maximum varies with the species.
To see how fast photosynthesis was induced when a leaf was exposed
to flashes of light, the researchers recorded measurements in the shade
and then opened a shutter that let in bright light. For each species the
scientists calculated the percentage of the maximum net photosynthetic
rate for a particular plant achieved after 1 minute of exposure to bright

light (see Figure 3A), which they called percent induction. They found
that the percentage induction after a 1 minute exposure varied among the
species. The amount of light available to the various rainforest species af-
fected their response to the simulated pattern of light that Pearcy and his
colleagues used. The shrubs that live beneath trees in the forest understory
had a significantly higher percent induction after being kept in the shade
before being exposed to bright light flashes. After 1 minute, these plants
had achieved a higher percentage of their maximum photosynthesis rate
than the other plants.
The percent induction also varied depending upon the length of a
shady period of time prior to exposure to 1 minute of bright light. There
was a lot of overlap in responses, but the clearing species consistently had
the lowest percent induction as the time in low light increased, much
more so than any of the other species.
Next, the researchers exposed leaves to bright light and then shade
and then bright light again. The net photosynthetic rate was measured,
as was the maximum response achieved after 1 minute of bright light.
Finally, they measured the light-flash use efficiency (LUE), where leaves
were subjected to flashes of light of increasing duration after a period
of shade and a period of bright light (Figure 4). LUE was calculated as
the amount of CO2 fixed by photosynthesis during a flash divided by
the maximum amount of CO2 fixed by photosynthesis under constant
bright light. If the ratio was one or close to one, then that leaf achieved
the maximum photosynthesis during the brief exposure to the flash.
LUE varied by species and by the length of the flash, and it depended
upon whether the leaf had been induced by bright light prior to expo-
sure to the flash.
The researchers found that the efficiency of use of light flashes was
extremely high. These are good adaptations for plants living mostly in the
shade and exposed to brief, but frequent, flashes of bright light through-
out the day. These plants and the plants living in the forest edge had
somewhat similar responses as the time in low light increased. The plant
that lived in clearings did not respond as well to light flashes. In fact, the
clearing species would not be predicted to do well in the understory or in
shady areas because of its lower induction and light use efficiency. Plant
250 leaves induced 250 leaves kept in shade
light flash use efficiency (% max photosynthesis)

with bright light and uninduced
= clearing
200 200
= edge
= understory
150 150
100 100
50 50
0 0
1 10 100 1 10 100
A length of flash (sec) B length of flash (sec)
Figure 4 LUE as a function of the duration of light flashes. A, Values

for leaves that had been induced with high light intensity to produce
maximum photosynthesis response, followed by a period of time in
shade, prior to light flash exposure. B, Values for leaves that had not
been induced prior to light flash exposure.
Source: From Valladares et al., 1997, Figure 6.
distributions, or where plants are found, are affected by the adaptations

that plants have to the amount and pattern of light available.
Aquatic plants are also adapted to varying light conditions. Bowes
and his colleagues sought to determine the limits to the growth of an
aquatic plant under different light conditions. The plant they worked
with was hydrilla (Hydrilla verticillata), which was introduced into the
southeastern United States and now is a serious weed problem in many
lakes. Hydrilla became a serious weed problem in less than 15 years after it
was introduced in Florida. It spreads rapidly and overgrows native aquatic
plants. To understand how it has been able to spread, scientists sought to
understand its adaptations to environmental conditions, including light
levels. Bowes and his colleagues designed an experiment to determine the
lowest light level at which hydrilla might be expected to survive and grow;
this is information that could be used to predict its spread.
Bowes and his colleagues collected hydrilla from Orange Lake, Florida,
brought them to the laboratory, and planted them in aquaria. All aquaria
were exposed to 16 hours of light each day, but each aquarium was exposed
to one of four light levels: low, medium-low, medium-high, and high. Each
week, the researchers removed several plants from each aquarium and mea-
sured their dry mass after all of the water was removed by placing the plant
in an oven. The researchers also measured photosynthetic and respiration
rates on living plants 3 weeks into the experiment. For this, they used
changes in CO2 levels as a proxy for photosynthesis, relative to the amount
of chlorophyll in the plant, and measured CO2 uptake at different light
levels.
In darkness, respiration of plants exceeds photosynthesis, so CO2
will be given off by the plants instead of taken up. As light levels increase,
photosynthesis will increase until it reaches a maximum rate, as indi-
cated earlier. When measuring changes in CO2, researchers must keep
in mind that this is net photosynthesis. When the net change is zero, the
two processes are in balance. Over the long-term, total photosynthesis
must exceed respiration, and the net photosynthesis must be positive for
the plant to grow and reproduce. A net photosynthesis of zero means
that the plant is photosynthesizing just enough to offset energy used in
cellular respiration. Bowes and his colleagues determined the light level
required to balance photosynthesis and respiration, and they also deter-
mined the light level at which maximum net photosynthesis occurred
for plants grown under different light levels (Table 3).
Growth of plants, as measured by changes in dry mass in plants col-
lected each week, were compared among the four light level treatments to
which plants were exposed. At the lowest light level tested, the change in
Table 3 Photosynthetic and respiration characteristics of hydrilla

plants grown under several light levels. Light levels are Einsteins/
m2/sec, and rates are moles of CO2/mg chlorophyll/hour. Values from
first two columns are estimates from a best fit curve of CO2 change
versus light level, and values from last two columns are means of
6 plants 6 1 SD.
light level where light level of maximum respiration
light level photosynthesis = maximum photosynthesis rate in
respiration photosynthesis rate darkness
low 7 150 2.6 0.3 1.2 0.9
medium-low 10 200 3.3 0.4 1.4 0.2
medium-high 15 350 4.3 0.2 2.0 0.3
high 20 600 5.4 0.6 2.5 0.2
Source: From Bowes et al., 1977, Table 1 and Figure 1.

mass was negative even after 3 weeks, suggesting that plants spent more
energy in respiration than they gained from photosynthesis. Plants at all
other light levels gained mass, but the amount gained increased with light
level and time.
Bowes and his colleagues concluded that the distribution of hydrilla
appears to be limited by low light levels, even though there is a large de-
gree of physiological compensation that plants can undergo to live in a
range of light conditions. Although the growth of the plant was negative,
hydrilla could still adjust its physiology to reduce both its photosynthetic
capacity and its respiration in the dark, as Table 3 shows. It takes in less
energy, but it is also able to decrease its energy use so that it burns less
energy. Plants in this treatment were also more responsive to low light in
a fashion similar to plants living in the rainforest understory. In terms of
its distribution, hydrilla may have a wider distribution and may be a bet-
ter competitor in lakes, because it has tolerance to low light conditions.
Hydrilla evolved to grow in a wide range of light conditions, and this may
facilitate its ability to spread to new habitats.
The amount of light affects the distribution of rainforest shrubs and
an aquatic plant. For the latter, even though the tolerance to varying light
is high, its distribution is limited by extremely low levels of light. Al-
though it might be predicted that plants that receive more light would
benefit from this high light, plants tend to do best when exposed to the
conditions to which they have adapted over evolutionary time. In this
way, they may avoid the costs associated with growing very large, because
it takes a large amount of energy and may take a long time to grow tall
enough to outcompete other trees for light.
Bibliography
Bowes G, Van TK, Garrard LA, et al.: Adaptation to low light levels by
hydrilla, J Aquat Plant Manage 15:3235, 1977.
Valladares F, Allen MT, Pearcy RW: Photosynthetic responses to dynamic
light under field conditions in six tropical rainforest shrubs occurring
along a light gradient, Oecologia 111:505514, 1997.
CHAPTER 4
Organisms in Ecological
Communities have Adapted
to Disturbance
Ecological systems rarely remain unchanged over time, despite the com-
mon misconception of the balance of nature. A lot depends upon the
scale at which the system is viewed. A forest may appear to not change
over time from one observers perspective, but a human observer has a
shorter lifespan than many trees. Careful observation reveals that even
a forest changes given enough time, especially when subject to a distur-
bance, which is a short-term change in the usual environmental con-
ditions that causes a change in an ecological system. Some ecological
systems are subject to frequent disturbance, including coastlines, flooded
streams, and forests subject to fires. Over time, natural selection would
result in adaptations for resisting or tolerating the disturbance. Natural
selection may be strong or weak depending upon the frequency of the
disturbance relative to the lifespan of the organism in question.
The types, frequency, and intensity of disturbance vary with the eco-
logical system. Forest fires in moist tropical forests have historically been
rare, although humans have set many fires in those ecological systems
in recent decades as a means to clear land for agriculture. It is unlikely
that species living in those forests are adapted to resist or tolerate fires.
Conversely, many forests in the western United States experience an an-
nual dry season during which the probability of fire is high. Fires do not
occur every year, but they do occur with high enough frequency that an
individual tree may experience many fires during its lifetime.
Many animals also experience fire in such ecological systems, even if
they have short annual life cycles. Aquatic organisms that live in streams
may be subject to flooding during annual rainy seasons or occasional

strong storms. These organisms experience increased water volume, ve-
locity, and turbulence. Marine organisms that live on rocky shores in the
intertidal zone (such as, starfish, algae, barnacles, and snails) are subject to
nearly constant wave action when the tide is high and drying conditions
when the tide is low. Frequent disturbance can act as an agent of selection,
leading to evolution of adaptations to resist or tolerate the disturbance.
Ecologists have studied the adaptations of species in ecological systems
subject to frequent disturbance.
Organisms can Adapt to Fire

A savanna is a tropical or subtropical woodland ecosystem. Trees on the
savanna are typically small and widely spaced, such that sunlight reaches
the layer of grasses and small shrubs. Savannas are seasonal ecological
systems with a distinct wet and dry season. Although annual rainfall may
be high, most of it occurs in one season. A long dry season makes savan-
nas susceptible to fires, which can quickly whip through dry grasses. Fires
in savannas are typically low in intensity with flames a couple of me-
ters high. An individual site experiences fire every 1 to 5 years. Contrary
to what might be expected, fires may be more intense in savannas that
receive more rain, because those habitats tend to produce more dense
stands of grasses that, when dry, provide more fuel for fires. This in turn
may affect the growth and evolution of trees.
Trees in fire-prone areas are known to have thick bark, which resists fire,
and branches well above the average height of flames from a fire. Seedlings
and young trees are more vulnerable to fire, because they may be only as tall
as the grasses and have not had time to develop thick, fire-resistant bark.
Gignoux and his colleagues determined the responses and adaptations of
young trees to fire. They worked in a savanna in Africa that experiences fire
annually. The two species they studied were the ordeal tree (Crossopteryx
febrifuga) and the monkey bread tree (Piliostigma thonningii). The ordeal
tree has scaly bark and grows to about 9 or 10 meters high, and the monkey
bread tree has rough, fissured bark and grows to about 15 meters.
For each species, Gignoux and his colleagues measured all of the indi-
vidual trees on five plots. They mapped their location, tagged them, and
ORGANISMS HAVE ADAPTED TO DISTURBANCE 37
measured their height and number of stems coming up from the ground.
New stems grow each year from surviving roots, even if an older stem
is burned up. The researchers classified each individual as a seedling, a
resprouted stem, or an adult. All of this was done in the early part of the
dry season, before the annual fire season.
The researchers also performed an experiment on twenty young trees
of each species. Next to each tree they erected an aluminum pole with
metal tags hanging at different heights. Each tag contained marks of
paints that changed color when exposed to a particular temperature. In
this way they could determine the temperature to which any tree was
exposed at each height. At the height of each tag, they also measured the
diameter of the tree as an index of resistance to fire, using the logic that
larger diameters are indicative of thicker barks and would lead to greater
resistance than smaller diameters. They predicted that larger trees would
have high survival when exposed to high temperature. However, they
could also determine whether small trees could survive high temperatures
indicative of fires. If the line of lethal temperatures was shifted to the left
on a graph of temperature vs. diameter, that indicates a tree species that
can survive high temperatures even when small, although the very small-
est ones would not survive.
Young trees not much taller than grasses are more susceptible to fire
than mature trees. Below a certain diameter, even low temperatures could
kill a stem or part of a stem. Frequent burning in the savanna has led to
the evolution of several adaptations useful for surviving in the presence
of fire. The researchers found that for each tree species there were trees
or parts of trees that were thick enough to survive even the hottest fire
they could measure. Once a tree gets past a certain size, thick bark, high
branches, and loss of leaves during the dry season are adaptations that
both savanna tree species possess. However, the ordeal trees line of lethal
temperature is further left than for the monkey bread tree, indicating that
the ordeal tree is better adapted to surviving fires when smaller.
One way that trees in the savanna have adapted to the regular dis-
turbances caused by fires is by resprouting stems from surviving roots
of burned-up trees. After a fire, the scientists measured the height of the
highest living branch and the diameter of the trunk at that height. The
measured total height achieved by each resprouted stem can be used as
a measure of the growth rate. The researchers graphed the cumulative

frequency distributions of resprouted stem heights to compare the two
species. The cumulative frequency distribution is a way of summarizing
tree height data by graphing the proportion of trees whose height is less
than or equal to a given value.
The researchers could use the current height of the trees to estimate
their growth rate, because all resprouted stems had been growing since the
last fire and because they all started at a height of 0 cm. The distribution of
ordeal tree heights is shifted to the left of the monkey bread tree distribu-
tion, which means that all resprouted ordeal trees were shorter than about
40% of resprouted monkey bread trees. From these data the researchers esti-
mated that the monkey bread tree grows 2.26 times as fast as the ordeal tree
Many other tree species living in fire-prone habitats also have some
or all of these adaptations, which is an example of convergent evolution,
a process in which organisms evolve similar structures or functions, even
though the species are not closely related evolutionarily. Unrelated species
exposed to the same selection pressures may evolve similar adaptations.
They may also evolve different strategies for dealing with the pressure.
In the two savanna trees, adaptations expressed in adults were similar,
but young trees possessed one similar and two different adaptations for
dealing with fire. Although each species could resprout stems from roots
that had survived a fire, the monkey bread tree grew faster, and the ordeal
tree was more resistant to high temperatures when small. More small ordeal
tree stems survived higher temperatures than did monkey bread trees of the
same size. If a monkey bread tree stem can grow fast enough to become
taller than grasses in between successive fires, there is a good chance that
stem will survive to become a mature tree. Although ordeal tree stems grow
slower than monkey bread tree stems, the lower, thicker part of a stem may
survive fire, allowing it to begin growing again, whereas a monkey bread
tree may have to begin growing a new stem from the ground up after a fire.
Organisms on Rocky Shores are

Adapted to Regular Disturbance
Marine animals living in intertidal zones are also subject to frequent dis-
turbance, yet waves and tides are more frequent than fires in savannas.
Intertidal zones are coastal areas that are underwater during high tide
and exposed to air during low tide. The habitats in these zones can be
wetlands, beaches, or rocky outcrops. The salt content of the water may
change from near freshwater when exposed areas above the tide receive
rain to extremely high salt content when water in tide pools evaporates.
Temperatures can also vary dramatically during low tide, depending on
air temperature and sun exposure. On rocky outcrops, waves can dislodge
or smash animals and algae attached to rocks. The intensity and frequency
of wave disturbance and fluctuations of salt and temperature depend
upon location between the lowest low tide and the highest high tide.
Some animals have adaptations for living in conditions in which these
disturbances are frequent, and these animals interact with each other in
these ecological systems.
To prevent themselves from being washed away, many organisms liv-
ing in rocky intertidal zones attach themselves to the rocks. Some mus-
sels, shelled animals related to clams, secrete protein threads from their
base, and the threads stick to the rocks. Many such threads together make
a strong attachment in the same way that many threads can make a strong
rope even if one thread is not strong by itself.
Two mussels that live along the rocky shores of Washington State are
the California mussel (Mytilus californianus) and the blue mussel (Mytilus
edulis). The blue mussel lives in a wide range of intertidal depths, but it
is most often found about 3 meters above the mean low tide height. The
heavier California mussel occupies the rocks from about 1 to 3 meters
above the lowest low tide mark, although it can be found in deeper
waters. To use their secreted protein threads, mussels must have space on
the rocks, and space may be a limiting resource. When on the same rock,
the California mussel can overgrow and crush the shell of the blue mus-
sel, thus displacing the blue mussel and gaining more space. Both species
are capable of withstanding strong wave action, and there may be some
overlap in where the two species can exist, yet they primarily exist in non-
overlapping intertidal zones.
Suchanek studied these two mussels to determine the reproductive
strategies and adaptations that allowed them to flourish in this highly
disturbed habitat where competition for space, predation by roaming
marine snails, and strong disturbances limit where each species lives.
He observed growth rates, sizes, and reproductive spawning events of

individual mussels.
Suchanek measured the mass of gonads, organs that produce gametes,
or eggs and sperm, of mussels relative to their shell length. Larger go-
nads are capable of producing more gametes. Suchanek reviewed research
done by other scientists to determine the spawning season of each species,
which is when massive numbers of eggs and sperm are simultaneously
released into the environment. Spawning can also be sporadic with fewer
individuals shedding gametes.
The literature review revealed that the California mussel releases gam-
etes throughout the year. The blue mussel releases gametes once a year,
spawning in the winter and early spring, which may also be a strategy for
living in this area of frequent disturbance; the larvae may have a better
chance of survival in the cooler winter and spring temperatures. Larvae
settle on unoccupied rocks in winter, and because they grow more quickly
than the California mussel at equal height above the tide, early on in
development they have a good chance of maintaining themselves at least
until they can reproduce once.
Suchanek next compared the shell lengths and masses of the two mus-
sel species. The earliest age of reproduction was determined by noting the
presence of mature gonads in mussels whose lengths had been measured
and that had been collected from patches colonized on a known date.
Lifespans of mussels living in different zones were either directly mea-
sured over time or inferred from growth rate data and maximum shell
length. Finally, the scientist analyzed the tolerances for various physical
conditions of the environment.
The two mussel species studied by Suchanek have different strategies
for dealing with disturbances and species interactions in the context of
the rocky intertidal ecological system. Although the rate of growth in
mussels is dependent upon food availability and height above the low tide
mark, when the two species initially colonize a bare patch on the rocks,
they still differ in their shell weight/length ratio and their growth rates.
The blue mussel is smaller with a thinner shell than the California mussel,
which may make the blue mussel more susceptible to waves and preda-
tion. Because it lives higher up above the tides, there are fewer waves and
predators. In addition, this strategy allows it to avoid much competition
from the larger, heavier California mussel. But mussels are filter feeders
and feed on microscopic organisms floating freely in the water, and they
can only feed when they are under water. Populations of blue mussels that
live lower down in the intertidal zone are subject to more disturbance,
predation, and competition. But access to more food resources may allow
them to grow faster when submerged below the high tide.
The California mussel lags behind in early growth rate and in the time
it takes to reach sexual maturity. Ultimately, they achieve a larger size and
possess a heavier and thicker shell than blue mussels of the same size.
This allows the California mussel to live in a zone of the intertidal that
is subject to more disturbance and predation. The large thick shell of the
California mussel makes it more difficult for starfish and snails to prey
upon it and waves to break it apart.
Ecologically, both species are limited in where they can live by the
height of the rocks above the tide and the associated heat and desiccation
that occurs in the summers when the tide is out. The blue mussel can live
higher up than the California mussel. It only lives lower down on rocks
unoccupied by the California mussel, and only in the narrow zone where
they overlap do they coexist for any length of time.
Species have adaptations for living in ecological systems subject to
frequent disturbance, and those adaptations evolved not only as a re-
sponse to the disturbances themselves but as responses to interactions
with the other species living in the system. Species evolve different strate-
gies that often involve differences in growth or reproduction, and there
is not one best strategy for dealing with disturbances; a variety of strate-
gies may evolve and lead to species survival. The strategy employed by
a particular species evolves in response to the disturbance and the other
species with which it interactsas a competitor, predator, or preyin
another example of possible coevolution.
Ethical, Legal, Social Implications:

Policy can be used to Help Prevent Forest Fires
Fire is a natural disturbance in many ecological systems, and species
living in these areas have adapted to fire. Which species live in forests
that occasionally or frequently experience fire will be determined by the
adaptations that those species have to fire of different intensities. For over
100 years, forest managers in the United States have used prevention of
fire as its main strategy. When a fire breaks out, the response by the US
Forest Service and other management agencies is to control it and elimi-
nate it as soon as possible. The 10 AM policy, instituted in 1935, stated
that fires were to be under control by 10:00 AM the day after they were
observed. This led to aggressive fire suppression. Is fire suppression the
best strategy for ecological systems and human communities?
In the absence of fire, a normally fire-disturbed community will
change. Plants that have strategies to regrow quickly after a fire will domi-
nate in fire-prone areas. These strategies include possession of large root
masses that can resprout stems after a fire, thick bark that resists burning,
and seeds that germinate after exposure to heat. These species can either
tolerate or resist heat and flames, and they will outcompete other species
that are not tolerant of fire. In the absence of fire, intolerant species may
outcompete tolerant species. The ecological benefits of fire include the
maintenance of species that would otherwise be outcompeted, preserva-
tion of biodiversity, increased rates of decomposition during and subse-
quent to a fire, control of tree diseases, and improvement of habitat for
forest animals.
In large areas where fire has been suppressed, changes have occurred.
The density of trees has increased, and the composition of species has
changed. There has been an observed shift toward less fire-tolerant spe-
cies. For example, in high elevation sites in the western United States,
Douglas fir (Pseudotsuga menziesii) and grand fir (Abies grandis) have been
expanding into areas that were previously dominated by ponderosa pine
(Pinus ponderosa). These areas have a high probability of dry season fires,
and fire naturally recurs every 1 to 12 years except when humans are sup-
pressing it.
Ponderosa pine has thick bark and the ability to self-prune, which is
where lower branches die and drop off. This latter trait produces a tree
that has all of its branches up high, lowering the probability that a fire will
spread to the tops of trees. In addition, they have deep roots and retain
moisture in their leaves. Seeds germinate quickly after a fire. Seedlings
grow well in the high nutrient soils created by fire. The fir and other trees
that are less fire tolerant have thinner bark and less heat resistant seeds and
seedlings. As the plant community changes, the animals that depend on

particular trees for food or habitat will also change.
Trees produce many seeds each year; when they germinate, many
thousands of seedlings begin to grow. These seedlings, regardless of the
tolerance to fire, are often the most susceptible life stages. In areas prone
to fire, many seedlings are wiped out each time a fire whips through. In
the absence of fire, many more seedlings survive, increasing the density
of trees in a forest. Giant sequoia (Sequoiadendron giganteum) groves have
been invaded by dense aggregations of white fir (Abies concolor) during the
era of fire suppression. Dead branches and trees begin to accumulate on
the forest floor. The longer that fire is prevented in an area, the more small
trees and dead wood accumulate. When fire does occur in such areas, it
will be more intense because there is more fuel to burn. Very intense fires
can then wipe out even fire-tolerant trees.
In recent years, as fires have been suppressed, more people have built
homes near forests. Suppression of fire in conditions of excessive tree
density and dead wood is very costly. The United States government
spent about $1 billion per year in the early 2000s to suppress fire. Despite
these expenditures, the acres burned has increased steadily from the mid-
1980s to the mid-2000s, and an average of six times as many acres have
burned at the end of that period as at the beginning of that period. It is
possible that the past policy of complete fire suppression caused a large
amount of deadwood that is fuel for a fire to build up in forests. This
might make fires burn hotter and be harder to control. Although there
is recognition that fire is a natural disturbance that maintains certain
ecological systems, there is much pressure put on governments to con-
tinue to suppress fires. That pressure comes from citizens living in or near
forests in fire-prone areas and from politicians that may not understand
the ecological benefits of fires.
Ecologists have begun to recognize the role of disturbance, and this is
beginning to affect policies and attitudes towards forest fires. A relatively
new policy tool in some areas is prescribed fire. These controlled burns
are now being used to reduce the amount of dead wood and seedlings in
forests where fires have been suppressed. A goal is to restore species that
have been reduced due to lack of fire. Giant sequoia forests have had very
little establishment of seedlings during the era of fire suppression, because
the seeds require fire to germinate. The heat from fire rises to the tops of
the trees, where it dries out the cones and causes release of seeds. The seeds
have a coating that needs to be burned off, after which they germinate in
the nutrient rich post-fire soil.
In addition to employing prescribed burns, the United States govern-
ment uses mechanical thinning, the physical removal of trees and dead
wood in dense forest stands, to help reduce the probability of intense fire.
Although prescribed burns cost about $125 per hectare, mechanical thin-
ning can be even more costly, upward of $2,500 per hectare. These are
costs to citizens, although the alternative of doing nothing may be even
more costly, both to the ecological systems and the human communities
living in the path of a raging fire.
A relatively new policy, enacted by the administration of President
George W. Bush, is to privatize mechanical thinning. In other words,
the logging industry would be given permission to cut in certain areas in
order to thin dense forests where fires have been suppressed. In return,
they would be allowed to profit from the wood they logged. There may be
some ethical issues with this policy if loggers are allowed to go into pri-
mary old growth forest and take prized, valuable and rare trees that would
have been protected from logging under another policy. There may also
be legal issues if the forest is in a protected area, and conservation groups
may object or initiate a lawsuit. However, if done wisely, this policy shift
may be a win-win-win for the logging industry, the taxpayers, and the
forests.
Bibliography
Donovan GH, Brown TC: Be careful what you wish for: the legacy of
Smokey Bear, Front Ecol Environ 5(2):7379, 2007.
Gignoux J, Clobert J, Menaut J-C: Alternative fire resistance strategies in
savanna trees, Oecologia 110:576583, 1997.
Suchanek TH: The role of disturbance in the evolution of life history strat-
egies in the intertidal mussels Mytilus edulis and Mytilus californianus,
Oecologia 50:143152, 1981.
Conclusion
In this book, evolution in the context of ecological systems has been
examined, including studies of individual species interactions and their
interactions with the abiotic environment. Evolutionary change occurs
at the level of the population, yet those changes do not occur in isolation
and in fact are contingent upon a variety of factors in the environment.
The themes of the evolution have been evident throughout this book.
Natural selection is the mechanism that accounts for adaptation to the
selective pressures of interacting species in the process of coevolution. Life
continues to evolve as the environment changes, and humans are a major
contributor to changes in our twenty-first century environment.
Glossary
adaptive. Showing or having a capacity for or tendency toward adaptation, as in
evolution by means of natural selection.
anthers. The part of the stamen, the male reproductive structure on flowering
plants, that contains the pollen.
carnivores. Carnivores are animals that eat animals.
coevolution. Coevolution is reciprocal natural selection of two or more species
where each species acts as a selective agent on at least one other species for traits
specific to their interaction.
communities. In ecology, communities are populations of species living in the
same place at the same time, that may or may not interact with each other.
convergent evolution. Convergent evolution is a process in which organisms
evolve similar structures or functions, even though the species are not closely
related evolutionarily.
coral reef. A physical structure composed of the calcium carbonate skeletons of
coral animals.
diffuse coevolution. Coevolution involving groups of species interacting with
other groups of species.
disturbance. A disturbance is a short-term change in the usual environmental
conditions that causes a change in an ecological system.
ecological systems. An ecological community together with the abiotic environ-
ment, usually considered to function as a unit.
endosymbionts. Organisms that live inside the cells of other species.
extrapolate. Extrapolation is the application of a mathematical model outside of
the range of data that were used to build the model equation.
gametes. The egg and sperm are haploid sex cells and are required for sexual
reproduction
genomes. The total DNA content of individual organisms.
habitats. The type of environment in which a particular kind of organism usually
lives.
herbivores. Herbivores are animals that eat plants.
interactions. Positive or negative associations between species that affect growth
and evolution of populations. They may take the form of competition, predation,
parasitism, commensalism or mutualism.
intraspecific competition. Competition for resources within a species, that is,
between members of the same species.
mutualism. A mutualism is a relationship between individuals of different species
in which both individuals benefit from the association.
48 GLOSSARY
natural enemy. An organism that uses other organisms as resources.

natural selection. Adaptive mechanism by which evolution takes place and is
often summarized as differential survival and reproduction.
net photosynthetic rate. Net photosynthetic rate is the rate of CO2 used during
photosynthesis minus the rate of CO2 given off during respiration.
nonadaptive. Evolutionary changes that are not adaptive in nature, as in genetic
drift.
pairwise coevolution. Coevolution involving only one species interacting with
only one other species.
parasites. Organisms that live on or in another organism.
pathogens. Pathogens are organisms that cause disease.
photosynthetic. Of or relating to photosynthesis, the process by which green
plants and some other organisms use sunlight to synthesize nutrients from carbon
dioxide and water.
pollination. A process that transfers pollen.
predators. Organisms that kill and feed on other organisms.
prey. Prey are organisms that are consumed by predators, either in whole or part.
selective agents. Factors that lead to differences in survival or reproduction and
cause natural selection.
Index
Adaptive, xiii Herbivores, 2
Algae, 18 Hydrilla verticillata, 31
and relative capacity, 24 distribution of, 33
Anthers, 3 photosynthetic and respiration
characteristics of, 32
Bad tenant model, 21
Behavioral bout, 4 Interactions, xiii
Intraspecific competition, 22
Carnivores, 2
Chlorophyll, 1819 Light-flash use efficiency (LUE),
Coevolutionary mutualism, 28 3031
Communities, xiii Lipid content and profitability, 15
Coral bleaching, 17
causes of, 2021 Mutualism, 2
endosymbionts, 18 Mutualistic algae, 22
larvae, 1819
microbes with small genomes, 1718 Natural selection, xiii
sea surface temperatures versus Nonadaptive, xiii
extent of bleaching, 20
threshold models, 2223 Parasites, 2
variations from long-term average Percent induction, 2930
temperature, 19 Photosensors, 28
Coral reefs, 18 Photosynthesizing organisms
Crummy landlord model, 2122 aquatic plants, 31
changing CO2 concentration, 29
Diffuse coevolution, 2, 1115 light affects distribution
of, 2733
Ecological systems, xiii light-flash use efficiency, 3031
Egg-laying events versus pollination percentage of maximum, 2930
events, 45 plant adoptions, 29
Endosymbionts, 17 respiration of plants, 32
Evolving threshold model, 2223 species of rainforest shrubs, 2728
Extrapolation, 20 Photosynthetic dinoflagellates, 17
Pollination, 2
Fixed threshold model, 22 events versus egg-laying events, 45
Predators, 1
Genomes, 17 prey race, 811
Graded threshold model, 22
Guam Marine Laboratory, 23 Relative yield fraction, 13
Ripe fruits, characteristics of, 12
Habitats, xiii overall profitability (OP) measure
Heat tolerance, benefits of, 23 of, 1213
50 INDEX
Sea surface temperatures, 24 Tegeticula yuccasella, 4

Species, evolution of, 12 Tetrodotoxin, 89
coevolutionary mutualism, 28
diffuse coevolution, 1115 Yucca kanabensis, 4
predator-prey race, 811 Yucca plants, 23
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FOR THE inCommunities

Christopher J. Paradise, PhD

All rights reserved. No part of this publication may be reproduced, stored

First published in 2016 by

ISBN-13: 978-1-60650-967-8 (print)

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Cover and interior design by S4Carlisle Publishing Services Private Ltd.,

Printed in the United States of America

This book about evolution of interactions in ecological communities

Terrestrial ecological systems are recognizable most easily by the types

Species have Evolved as

Leaving after collecting pollen is an adaptation that has little apparent

amount of pollen received by flowers from 4 to 5 pollinations, and the

Relating these results to the previous studies of moth behavior, moths

A Predator-Prey Arms Race

arms race characterized by the evolution of tetrodotoxin and resistance to

time (min + 1 SE)

Figure 1 Responses of garter snakes to newts. A, Percent resistance

percent resistance to tetrodotoxin was related to the categories of how the

newts. Even when exposed to newts from a population with generally

proportion of the fruit pulp that is water, 1 WP is the proportion of

Corals are Bleaching

Table 1 Microbes with small genomes, compared to E. coli.

Source: From http://www.ncbi.nlm.nih. gov/genomes/lproks.cgi

population. If a microbe deleted a gene that it no longer needed, then

photosynthetic pigment called chlorophyll fluoresces red when stimulated

However, McWilliams and his colleagues found that the log-

Figure 2 Global coral bleaching in 2007. A, Qualitative data from

their color, what remains is the white, calcium-rich exoskeleton of the

symbionts. Remember that endosymbiotic genomes tend to get rid of

Table 2 Comparison of two species of algae and their relative capacity

Source: From Rowan, 2004, Figure 1a.

Roberts L: Corals remain baffling, Science 239(4837):256, 1998.

The Amount of Light

Evolutionary processes can be better understood by exploring how a

(moles of photons/m2 1 SD) 20 100

intensity periods ( 1 SD)

% received during high

Figure 3 Properties of the light environment in the forest understory

rate for a particular plant achieved after 1 minute of exposure to bright

250 leaves induced 250 leaves kept in shade

light flash use efficiency (% max photosynthesis)

Figure 4 LUE as a function of the duration of light flashes. A, Values

distributions, or where plants are found, are affected by the adaptations

Table 3 Photosynthetic and respiration characteristics of hydrilla

Source: From Bowes et al., 1977, Table 1 and Figure 1.

may be subject to flooding during annual rainy seasons or occasional

Organisms can Adapt to Fire

a measure of the growth rate. The researchers graphed the cumulative

Organisms on Rocky Shores are

He observed growth rates, sizes, and reproductive spawning events of

Ethical, Legal, Social Implications:

seedlings. As the plant community changes, the animals that depend on

natural enemy. An organism that uses other organisms as resources.

Sea surface temperatures, 24 Tegeticula yuccasella, 4

Behavior and Information Exchangeby Christopher J. Paradise and A. Malcolm Campbell

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