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Population growth, dynamics, and blooms of bacterial, unicel-
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Microbes are used to illustrate both exponential and logistic
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harmful algal blooms. Populations of harmful algal can quickly
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Biology Christopher J. Paradiseis professor of biology and environ-
Mathematics mental studies at Davidson College. He teaches introductory
Chemistry biology, ecology, entomology, and topical seminars on ecotoxi-
cology and renewable natural resources. He also occasionally
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A. Malcolm Campbell
Ecological Dynamics
Ecological Dynamics
Christopher J. Paradise, PhD

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

in a retrieval system, or transmitted in any form or by any means
electronic, mechanical, photocopy, recording, or any other except for
brief quotations, not to exceed 250 words, without the prior permission
of the publisher.
First published in 2016 by

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ISBN-13: 978-1-60650-957-9 (print)

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Abstract
Population growth, dynamics, and blooms of bacterial, unicellular
eukaryotes, and toxic algae are described in this book. Microbes are used
to illustrate both exponential and logistic population growth. Microbes
are also used to illustrate dynamics in other aspects of ecological systems,
including nutrient cycling. The movement of nitrogen in ecological sys
tems is largely affected by microbes, some of which have symbiotic rela
tionships with legumes. The effects of the environment on the growth
of microbes and the effects of the microbes on ecological systems are
described in reference to nutrient cycles and harmful algal blooms. Popu
lations of harmful algal can quickly grow and exceed carrying capacity,
with resulting negative effects on other species, including humans.
Keywords
organism, dynamics, populations, ecological systems, paralytic shellfish
poisoning, microbes, doubling time, growth rate, exponential growth,
carrying capacity, logistic growth, protists, nitrogen fixation, nitrogen
cycle, assimilation, decomposition, nitrification, denitrification, algal
bloom, red tide, phytoplankton, harmful algal bloom, iron hypothesis,
zooplankton, ocean fertilization
Contents
Preface...................................................................................................ix
Acknowledgments....................................................................................xi
Introduction.........................................................................................xiii
Chapter 1 Populations of Unicellular Organisms can
Increase Over Time............................................................1
Chapter 2 Soil Microbes are Involved in Nutrient Cycling................11
Ethical, Legal, Social Implications: There are
Positive and Negative Consequences of
Agricultural Practices on Soil Ecosystems......................23
Chapter 3 Certain Phytoplankton can Produce a Red Tide...............27
Ethical, Legal, Social Implications: Seeding the
Oceans with Iron to Increase Productivity and
Create a Carbon Sink has Consequences.......................39
Conclusion............................................................................................43
Glossary................................................................................................45
Index....................................................................................................47
Preface
This book about ecological dynamics, or change over time, is part of a
thirty book series that collectively surveys all of the major themes in bio
logy. Rather than just present information as a collection of facts, the reader
is treated more like a scientist, which means the data behind the major
themes are presented. Reading any of the thirty books by Paradise and
Campbell provides readers with biological context and 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 entire 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 ecological dynamics 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 ecological dynamics the way professional scientists
dowith experimentation and data analysis. In short, data are put back
into the teaching of biological sciences.
Readers of this book who wish to see the textbook version of this
content can go to www.bio.davidson.edu/icb where they will find
pedagogically-designed and interactive Integrating Concepts in Biology for
introductory biology college courses or a high school AP Biology course.
Acknowledgments
Publishing this book would not have been possible without the generous
gift of Dr. David Botstein who shared some of his Breakthrough Prize
with co-author AMC. Davids gift allowed us to hire talented artists
(Tom Webster and his staff at Lineworks, Inc.) and copyeditor Laura
Loveall. Thanks go to Kristen Mandava of Mandava Editorial Services for
project management and guidance. In particular, we are indebted to Katie
Noble and Melissa Hayban for their many hours and attention to detail.
Kristen Eshleman, Paul Brantley, Bill Hatfield and Olivia Booker
helped us with technology at Davidson College. We are grateful to
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 Inte-
grated 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
In another book in this series, it was shown how individual cells could
disrupt the function of other cells. Despite the focus on the individual,
no cell exists in isolation. Biologists study cells from the molecular to the
whole organism, and in this book, the focus is on dynamics of popula-
tions and ecological systems using populations of cells as the model of
study. Unicellular organisms live in populations and have characteristic
population growth and dynamics.
These populations of single-celled organisms can affect an entire
ecological system. In 2005, the toxic unicellular organism Alexandrium
fundyense forced the closure of New England shellfish beds. This species
caused the largest red tide in that area in over 30 years. Officials
warned that eating shellfish contaminated with the toxin produced by
this organism could cause paralytic shellfish poisoning (PSP). The
same year in Florida, the biggest bloom since the 1970s of a related
unicellular organism, Karenia brevis, caused massive fish kills, death of
manatees, and respiratory complaints from beachgoers. Some blooms
are far enough offshore that we cannot see them, yet they can have
wide-ranging effects on the coastal marine ecological system and on
terrestrial organisms living close to the shore. Unicellular organisms
can play other roles in ecological systems and some microbes are
essential in the cycling of nutrients and the fixation of nitrogen. In the
description of these phenomena the themes of the cell concept are seen:
All cells come from preexisting cells, cells maintain internal environ
ments that differ from external environments, cell structure defines cell
function, and cells communicate with other cells.
CHAPTER 1
Populations of Unicellular
Organisms can Increase
Over Time
Both prokaryotic and eukaryotic cells divide, although the methods

differ. Bacteria and archaeans are prokaryotes and all other organisms
are eukaryotes. Most unicellular organisms reproduce by cell division
binary fission in prokaryotes and mitosis in eukaryotes. The population
growth rate of unicellular organisms is one way to characterize and com
pare species and to quantify positive and negative environmental effects
on cells. C. Kelly and Otto Rahn wanted to compare the doubling time,
the time it takes for a population to double in number, and variability in
cell division time of two species of bacteria: Bacterium aerogenes, Bacillus
cereus, and a yeast, Saccharomyces ellipsoideus. The investigators placed bac
teria onto agar plates. They cut a square out of the agar gel and watched
individual bacterial cells under the microscope. They observed individual
cells growing on a block of agar for as long as they could identify indi
vidual parent and daughter cells, about four generations (shown for
S. ellipsoideus in Figure 1). The scientists monitored the small population
of cells every 5 minutes and noted when any cell divided. Once the popu
lation became too dense, observations of individual cells were impractical.
Results from one experiment showing the second, third, and fourth
generations are shown in Figure 2A. The scientists repeated this experi
ment many times for each species and pooled the data across generations
and replicates of the experiment (Figure 2B). Out of 110 such experi
ments, they noted that three first generation cells did not divide; all others
did. Once a cell began to divide, all of the daughter cells also divided for
as long as they recorded data.
2 ECOLOGICAL DYNAMICS
I first generation cell

original parent cell time 0 for first division
0
second II I II second generation cell

generation cell 95 0 95 time for second division
fourth generation cells time for fourth division
0
25
30
25
36
5
III II I II III
255 180 95 0 95 190 255
III III
180 190
time for
0
third division
25
third
30
5
generation cells
Figure 1 Schematic of cell division for bacteria and yeast observed on

agar plates under microscope. The shaded cell is the original parent cell;
its first division yielded one offspring cell (A). The second generation
is shown in B, and the third and fourth generations are shown in C.
Roman numerals indicate the generation and Arabic numerals number
of minutes, in 5 minute increments, for the indicated cell to appear.
Each cell, including the parent cell, divided in each generation.
Source: From Kelly and Rahn, 1932, Figure 3.
The first generation of cells in the population depicted in Figure 2A con

sisted of eight cells that all divided between 5 and 20 minutes after observa
tions began. All cells lived and continued to divide, meaning there were 16 cells
at the end of the second generation, 32 after three generations, and 64 after
four. The cells in the second generation took between 20 and 45 minutes to
divide. To determine the size of the population after three generations, it is
simple to multiply 8 2 to get 16, 16 2 to get 32, and 32 2 to get 64.
The number of cells after n generations can also be written, x = 8 2n,
and this is better than multiplying by 2 over and over, because the num
ber of cells after 10 generations (= 8 210 = 8192) or 20 generations
(=8 220 = 8, 388,608) can be found without knowing the number of
cells in any other generation. There is also a formula that can predict the
number of cells after a certain amount of time, regardless of the number
of generations that have passed.
For a population that starts with x0 cells and divides every T minutes,
the number of cells after t hours is modeled by x = x0 260/T t. For
example, when a population starts with 8 cells and divides every
Populations of Unicellular Organisms can Increase Over Time 3
50
= 2nd
percentage of cells dividing

40 = 3rd
= 4th
30
20
10
0
A 10 15 20 25 30 35 40 45
25
= Bacteria aerogenes
percentage of cells dividing
20 = Bacillus cereus
= Saccharomyces ellipsoideus
15
10
0
0 10 30 50 70 90 110 130 150 170
B time (min)
Figure 2 The proportion of cells dividing within a particular period of

time for a single small population of Bacterium aerogenes tracked over
four generations (A) and three species of bacteria, with data pooled
across generation and population (B). In A, second, third, and fourth
refer to the generation.
Source: From Kelly and Rahn, 1932, Tables 1-4, original art.
20 minutes, x = 8 260/20 t = 8 23t. The multiple of t in the exponent

is the number of generations per hour, or growth rate, the change in
number of individuals per unit time. The doubling time is the number of
hours per generation, or T/60, which is the reciprocal of the number mul
tiplying t in the exponent. For example, if x = 8 25t, then the doubling
time is 1/5 of an hour or 20 minutes.
Kelly and Rahn showed that individual bacterial cells rarely suffer
mortality under optimal laboratory conditions. Cells divide and continue
to divide at a mean rate, determined by the conditions and the species.
If all cells divide each generation, and the growth rate is the same across
generations, then in each generation there will be two new daughter cells
for every one dividing cell, regardless of the number of cells present. The
growth rate of the population would be constant and is calculated by
determining how many new individual cells are produced per individual
already present in the population per hour. For the example of a popula
tion with a doubling time of 30 minutes, the original cell will produce
one new cell in the first 30 minutes, and then the original cell will divide
again, producing one more cell. Therefore, the growth rate is 2.0 indi
viduals per individual per hour.
The growth modeled here, in which cells double at regular intervals,
is called exponential growth. A feature of exponential growth is that
it looks linear when plotted on a logarithmic scale, and the population
growth rate can be estimated as the slope of that line.
The time it takes for an individual cell to divide varies within the spe
cies, and the average time for the entire population to divide is specific
to the species. Individuals of Bacillus cereus and S. ellipsoideus exhibited
much more variability in dividing times than Bacterium aerogenes; cells
of both former species had division ranges of over 2 hours, whereas all
Bacterium aerogenes cells divided within 75 minutes.
Because the data in Figure 2B is in the form of a relative frequency
distribution, the weighted average method can be used to estimate mean
doubling time of the two species. Weighted sums of approximately
32.7, 51.4, and 109.7 minutes were obtained for the doubling times of
Bacterium aerogenes, Bacillus cereus, and S. ellipsoideus, respectively. Each
Bacterium aerogenes cell divides in two, producing one new individual
every 32.7 minutes on average.
Bacterium aerogenes has a shorter doubling time than Bacillus cereus or
S. ellipsoideus. As long as there is no mortality, starting with a population
of 8 individuals of Bacterium aerogenes, the population would consist of
64 individuals at the end of three divisions or generations, and it would
take, on average, 3 32.74 = 98.22 minutes to achieve that population
size. It also has a growth rate of 1.83 individuals per individual per hour,
which is obtained from the model presented above (32.74 minutes

1 hour/60 minutes = 0.546 hours and 1/0.546 = 1.83).
Scientists have described bacterial growth under ideal conditions,
going beyond simple counts of small numbers of cells in the microscope,
and most bacterial cultures (even in optimal conditions) do not always
grow in the manner just modeled. Aditya Mittal and his colleagues stud
ied growth of the bacterium E. coli in cultures (Arora et al. 2007). The
scientists grew cultures in flasks until the cell density gave an absorbance
reading of 1.0 on a spectrophotometer. Spectrophotometry can be used
to estimate the density of cells in a sample because the cells scatter and
absorb light, preventing it from being detected on the other side of the
test tube. This method provides a repeatable way of estimating cell den
sity, because more cells cause more scattering and absorbance of light.
The cultures that Mittal and colleagues grew were then used to inocu
late fresh 250 mL cultures. They placed 5 milliliters of the inoculation
culture into 250 mL of fresh liquid media that contained all the nutrients
required for growth. Replicate cultures were grown at 37o C. Shaking of
the flasks ensured that the bacteria and the nutrients were well mixed.
Every 30 minutes the scientists collected a sample from each flask, placed
it in a test tube, and read its absorbance on the spectrophotometer. The
scientists developed a growth curve from the data using a best fit line. This
curve appeared to grow slowly at first, then grew exponentially, began to
slow down after about 5 hours and then went into what the researchers
described as a stationary phase after a little over 8 hours, where contin
ued growth was slow or near zero.
M. Zwietering and colleagues grew another bacterium, Lactobacillus
plantarum, at different temperatures and fitted curves to the population
growth data (Zwietering et al. 1990). The scientists grew the bacteria in
a liquid medium and at regular intervals took a subsample, which was
spread over the surface of an agar plate. Colonies grew from individual
starting cells, so the number of colonies equals the number of starting
cells. Back-calculating that number to the entire culture allowed the sci
entists to estimate the size of the entire population. As with E. coli, the
scientists found slow growth at first, then exponential for a period of
time, and then stationary, or zero growth, at very high population sizes.
The rate of growth during exponential growth and the final size of the
population, often both considered as constants for populations, were

shown to vary depending upon the temperature at which a culture of
L. plantarum was grown. At higher temperatures, both growth rate and
resulting carrying capacity were higher than at lower temperatures.
The growth curves in these bacteria are fairly typical of laboratory cul
tures. The populations cells are not growing exponentially the entire time,
but are going through a succession of phases in which they grow at dif
ferent rates. In the lag phase the population size is small and growth rate
is near zero. Then the population transitions to the exponential phase,
where growth rate is maximum and constant, and cells are growing
exponentially. Eventually the growth rates slow down, leading into the
stationary phase, when the population is large, but the growth rate is
again near zero. These three phases give a characteristic S shape to the
growth curve. The stationary phase may be followed by a death phase, in
which the population declines.
These kind of so-called logistic growth curves look similar to each
other, but they are distinctly different from exponential growth. The
exponential population modeled earlier had constant growth rate over
time; clearly these populations do not. There are conditions under which a
population of individual bacterial cells do not all divide or survive, which
were assumptions of the exponential growth model. Logistic growth is
more realistic than exponential growth in that respect.
Cells transferred from cultures in the stationary or death phase do not
begin to divide immediately and are known to go through a distinct lag
phase. This may be caused by depletion of various macromolecules that
individuals must rebuild prior to cell division. Lags are also known to
occur when cells have been injured, irradiated, or transferred into cultures
that have fewer nutrients than were present in their previous environ
ment. The lag observed by Mittal and colleagues was an artifact from
placing a small population in a large flask so that there was a lag before
absorbance was affected. In all likelihood, the bacteria in conditions with
high levels of resources and low population densities were all dividing in
a manner similar to that observed by Kelly and Rahn.
No population, whether bacterial, animal, or plant, can grow expo
nentially for long, which is why exponential population growth models
are less realistic than logistic population growth models. The stationary
phase occurs when a bacterial population runs out of an essential nutri

ent, causing cell division to cease, or when waste products build up in the
culture flask, causing toxicity. Cells may be able to survive for a period
of time, but they do not have the energy or resources to actively divide.
At some point, nutrients are so low or toxins are so concentrated, that
individual cells begin to die, marking the beginning of the death phase.
Populations of other organisms should also exhibit growth that
depends on environmental conditions. Consider populations of unicellu
lar eukaryotes, which belong to a group of organisms known as protists, a
diverse group of organisms. Protists are members of a group of eukaryotic,
mostly unicellular organisms, including algae and protozoans. Protists
have a relatively simple organization, relative to the other eukaryotic and
multicellular animals, plants and fungi, but different groups of protists
do not share much in common. Most are unicellular, but there are some
colonial species and some simple multicellular species. Some common
single-celled protists are Amoeba, Paramecium, green algae, kelp, and
Plasmodium. Among these organisms there are species that photosynthe
size, as well as species that are predators, pathogens, and detritivores,
which are animals that feed on dead plant or animal matter.
Unicellular protists live in almost every aquatic environment. Protist
populations reproduce asexually or sexually, and some species can employ
both modes of reproduction. Populations grow as individuals reproduce,
and this growth is an emergent property of individual reproduction.
Photosynthetic dinoflagellates, diatoms, and green algae are important
components of aquatic food webs, where their production forms a major
component of food for other organisms especially in the ocean. Dino
flagellates are responsible for red tides, which will be explored in more
detail in a later chapter.
The growth rate of unicellular protist populations such as dinofla
gellates may be studied in much the same manner as bacterial popula
tions. Two scientists, G. Dixon and P. Syrett, investigated the growth
of four species of photosynthetic dinoflagellates, Amphidinium carterae,
A. klebsii, Scrippsiella trochoidea, and Gyrodinium aureolum, under dif
ferent conditions in laboratory cultures (Dixon and Syrett 1988). All
cultures were maintained in special growing media in an incubator. The
scientists gently shook half the cultures of each of the four species to
simulate turbulence in the ocean. The control cultures were not shaken.
In addition, A. carterae was exposed to variation in type and concentra
tion of nitrogen-based molecule. The biologists removed a sample of each
culture every 1 to 3 days to estimate the population size over a 20-day
period. They counted a subsample of each culture and then scaled the
count to estimate the total population sizes in the original cultures.
When shaken, growth of A. carterae was unaffected and shaken and
unshaken cultures grew equally well. However, all individual cells in the
population of G. aureolum were dead after 8 days when the culture was
shaken. The two other species, A. klebsii, Scrippsiella trochoidea, grew
under both conditions but in each case growth rate was higher and the
final population size in unshaken cultures was greater than for shaken
cultures. It may seem odd that three of the dinoflagellate species had
lower growth when the cultures were shaken compared to when they
were not, considering that these dinoflagellates are often found in tur
bulent waters. Turbulence may affect the ability of individuals to gather
nutrients, although the scientists did not combine their nutrient and
shaking treatmentsall the cultures in the first set of experiments,
whether shaken or not, had very favorable nutrient conditions. Dixon
and Syrett suggested that the response to turbulence may slow down
algal blooms and because species responded differently, more or less
turbulent conditions could play a role in the outcome of competitive
interactions.
Populations of A. carterae were affected by both the type of nitrogen
and the concentration of ammonium ion present. Three of the four types
of nitrogen allowed for rapid growth of A. carterae, but the ammonium
ion allowed for high population growth only when present in low con
centrations. Populations of this dinoflagellate hardly grew at all at high
concentrations of ammonium. The scientists noted that the cells became
large, rounded, and non-motile. This abnormal morphology suggests
that ammonium may be harmful to the cells. As with other organisms,
dinoflagellate populations are affected by the environmental conditions
in which they exist, and this can affect their interactions with other cells
and their ability to reproduce.
The unicellular eukaryotic dinoflagellates exhibited very similar
growth curves to the bacteria examined earlier, at least under conditions
favorable to growth. As with the various bacteria species, some species

have higher growth rates than others. The dinoflagellates, even in opti
mal conditions, do not grow as fast as the bacteria examined earlier in
this chapter. However, the growth curves did contain exponential and
stationary growth phases. Some of the populations may have exhibited a
lag phase in the early part of the experiment, although existence of a lag
phase may be dependent on the growth conditions, just as in bacterial
populations. Poor conditions cause some populations to never enter an
exponential phase but rather go straight into a stationary phase or decline,
suggesting conditions that cause mortality of individual cells.
Growth rates in eukaryotes are lower than those in bacteria; it may
take several days to reach a population in the dozens for dinoflagellates,
whereas some bacteria populations can double every 20 minutes in the
right conditions. Like bacteria, all eukaryotic cells come from preexist
ing cells. Unlike bacterial populations where every cell divides within a
certain period of time, there is not much evidence that unicellular eukary
otes do the same. Eukaryotes are more complex in their cell structures
and usually larger than prokaryotes. Reproduction, including mitosis or
meiosis, is more involved than binary fission, and there may be more
variation among individuals in terms of whether they reproduce in any
generation. Regardless, population growth curves among these two very
different types of unicellular organisms may exhibit similar trajectories
under favorable conditions. The increase in complexity in eukaryotic cells
is partly due to the evolution of organelles, allowing compartmentaliza
tion of functions and increases in cell size. This increased complexity
allows for a diversity of cell structures and functions.
Bibliography
Arora S, Bhat V, Mittal A: Correlating single cell motility with popu
lation growth dynamics for flagellated bacteria, Biotechnol Bioeng
97(6):16441649, 2007.
Dixon GK, Syrett PJ: The growth of dinoflagellates in laboratory cultures,
New Phytol 109:297302, 1988.
Kelly CD, Rahn O: The growth rate of individual bacterial cells, J Bacteriol
23(2):147153, 1932.
Monod J: The growth of bacterial cultures, Ann Rev Microbiol 3:371394,

1949.
Zwietering MH, Jongenburger I, Rombouts FM, et al: Modeling of
the bacterial growth curve, Applied Environm Microbiol 56(6):
18751881, 1990.
CHAPTER 2
Soil Microbes are Involved

in Nutrient Cycling
Find a flower bed or vegetable garden and pick up a handful of soil.

Describe it. How does it smell and feel? What color is it? Is there any
thing living in the soil? Soil is a key component of any terrestrial eco
logical system. Healthy soil is necessary for plants to grow. Farmers often
add fertilizer to the soil to provide essential nutrients, such as nitrogen,
potassium, and phosphorus. How do plants obtain nutrients that may
be in short supply without help from farmers? Farmers have known for
many years that the crops grown on a plot of land affect the nutrient
levels available for subsequent crops and that when crops are harvested,
nutrients are removed from the system. An area of research that led to
discoveries with implications for interactions in ecological systems was
the variability in nutrient needs among different plants and the science
behind crop rotation.
R. Seneratne and G. Hardason performed a field experiment designed
to determine the effects of different crops on nitrogen levels in soils. The
three crops they worked with were faba bean (Vicia faba), pea (Pisum
sativum), and barley (Hordeum vulgare). Faba bean and pea belong to the
family of plants known as legumes, and barley is a type of grass. Seeds of
these three crops were planted in mid-April. Within the acreage of each
crop, Senartne and Hardason established multiple 3m 5m plots. The
researchers added ammonium sulfate ([NH4]2SO4) to each plot at a rate
of 20 kg/ha.
Each plot was subdivided into two areas: one was 3m 2m, and the
other was 3m 3m. Within the smaller half of each plot, subplots were
established. In these subplots the ammonium sulfate added contained a
stable isotope of nitrogen (15N). All plots also received potassium and
phosphorus in quantities that would prevent growth of plants from being

limited by these nutrients. Twelve weeks after the seeds were planted, all
of the aboveground plant material from the smaller half of the plot was
harvested and separated into pods, leaves, and stalks (for legumes) and
grain and straw (for barley). All of the material was dried, weighed, and
ground up. The percent of nitrogen in the different fractions was esti
mated, and these values were extrapolated to mass per hectare (Figure 3).
The researchers determined the relative ratio of 15N and 14N, which
allowed determination of the amount of nitrogen taken up by plants
during growth from fertilizer addition. Seneratne and Hardason deter
mined the amount of nitrogen obtained from the soil fertilizer and the
nitrogen fixation that occurred in each treatment (Table 1), which is
the difference between total nitrogen and nitrogen acquired from the
soil. Nitrogen fixation is the conversion of atmospheric nitrogen (N2)
to ammonia (NH3). They also determined the amount of nitrogen con
served for future crops relative to barley (Table 1). Because nitrogen
fixation for barley is zero, the difference between the soil nitrogen by
barley and that used by one of the other crops was defined as nitrogen
conserved for future crops.
120
= leaves/stalks
100 = pods/spikes
nitrogen content (kg/ha)
= total
80
60
40
20
0
faba bean pea barley
Figure 3 Nitrogen content of aboveground portions of crops.

Barley plots had either the same amount of nitrogen fertilizer
as faba bean and pea or three times as much (high N).
Source: From Seneratne and Hardason 1988, Table 2.
Soil Microbes are Involved in Nutrient Cycling 13
Table 1 Source of nitrogen for three crops. All values are

in kg/ha.
variable faba bean pea barley
total nitrogen content 113.3 107.9 56.6
nitrogen fixation 83.7 73.4 0
soil nitrogen used 29.6 34.5 56.6
nitrogen conservation 27.0 22.1
Source: From Seneratne and Hardason, 1988, multiple tables.
In the second part of the experiment, all of the plant material from the
larger portion of half of the plots, which was not harvested, was chopped
up and tilled into the soil, along with the roots, in that half of the plot. In
the other half of the plots, the aboveground portion of plants were har
vested, and only the roots were chopped up during tilling. One week after
harvesting the first crop, the researchers sowed sweet sorghum seeds in all
plots. After the seeds had germinated the subplot in the larger half of the
plot received 60 kg/ha 15N-labelled ammonium sulfate. The final harvest
was 15 weeks after planting, and total nitrogen was determined as before.
The scientists already knew how much soil nitrogen was fixed and
used by the three crops. Seneratne and Hardason estimated the amount of
nitrogen returned to soil in chopped up roots as 10% of the total above
ground nitrogen (in Figure 3) and the amount returned to soil in chopped
up stalks from the average value determined from harvested plants (77.1,
22.7, and 29.2 kg/ha for faba bean, pea, and barley, respectively). These
amounts were what were considered to have been added back to the plots
prior to growing sorghum. Some nitrogen was taken away in pods and
grains (the harvest), but after harvest and tilling, plots with legume crops
not only used less soil nitrogen, but those crops returned more of it to the
soil. For instance, faba bean led to 82.4 and 68.7 kg N/ha in sorghum for
roots and roots plus stalks treatments. Pea led to 74.5 and 68.4 kg N/ha
for sorghum in the two treatments, and barley grown first led to only 41.3
and 51.8 kg N/ha in barley roots and barley roots plus stalks treatments.
Nitrogen fixation usually refers to the biological process by which
nitrogen (N2) in the atmosphere is converted into ammonia (NH3).
Lightning can cause nonbiological nitrogen fixation, and there are other
nonbiological processes that can convert nitrogen to nitrogen dioxide
(NO2). As might be hypothesized, based on lightning being involved, the
conversion of atmospheric nitrogen to ammonia is an energy intensive

process. Most organisms do not have the ability to fix nitrogen, and thus
cannot directly incorporate atmospheric nitrogen into their amino acids
to build proteins and nucleotides to build DNA and RNA. Animals, for
instance, get their nitrogen from proteins in their food. Nitrogen fixa
tion is essential for life, and yet only some organisms possess the enzyme
nitrogenase, which catalyzes the reaction.
Nitrogen fixation occurred in plots with legumes, faba bean, and pea,
which Seneratne and Hardason determined by subtracting the amount of
nitrogen taken up in the soil from the total nitrogen content of the plants.
The remainder must have come from atmospheric nitrogen. The legumes,
which have higher total nitrogen, incorporated nitrogen from both the
soil and the atmosphere, leaving more nitrogen available in the soil for
future crops. Although both crops had higher total nitrogen content than
barley, faba bean had more in the stalks, whereas peas had more nitrogen
in the pod, which is the part that humans consume.
Atmospheric nitrogen fixation led to less soil nitrogen depletion,
more conservation of nitrogen, and more total nitrogen, which is valu
able to us. Not only is there less depletion of soil nitrogen on plots with
legumes, after the crop is harvested any residue left behind (such as, roots,
stalks, and leaves) has a higher amount of nitrogen than residue from
non-legume crops. This can reduce the amount of fertilizer a farmer has
to apply to his crops. The sorghum crops planted after the legumes had
higher total nitrogen than sorghum grown after barley.
Although this study was performed in the 1980s, it has been known
by agriculturalists for decades that most legumes can reduce the use of
fertilizers and that rotation of crops can increase the fertility of soil.
Clover, another legume, is often planted in fields in between harvested
crops. Nitrogen fixation followed by tilling of clover into the soil replen
ishes nitrogen in forms usable by plants that are not associated with
nitrogen fixation. Given that nitrogen fixation is energy intensive and
requires the enzyme nitrogenase, one might wonder how it is that nitro
gen fixation occurs in the presence of legumes. Are legumes actually fixing
nitrogen? Because of the importance of legumes in agriculture, scientists
more than a century earlier than Seneratne and Hardason were already
investigating this question.
bacteria in
nodules host cell
vacuole
uninfected
root cell
roots vascular tissue

(cutaway to
behind nodule)
Figure 4 Root nodules on legumes. Shading in nodule cells show areas

with bacteria. A, Root nodules in Lupinus polyphyllus. B, Close up of
dissected root nodule.
Source: From Taubert, 1891.
To begin addressing this question, scientists examined the anatomy of

legume plants. One of the earliest reports from the 1800s noted nodules
on the roots of a legume (Figure 4A). Nodules on different legume species
were examined by several researchers, including Edwin Fred and his col
leagues. These scientists dissected nodules from roots of several legumes,
including beans (Phaseolus vulgaris) and red clover (Trifolium pratense)
and examined them microscopically.
The scientists sliced nodules very thinly and prepared microscope
slides of the sections. They used a variety of stains to highlight various
cellular structures and look for signs of infection, because one of the
hypotheses about the nodules was that they were growths caused by bac
teria. Using a stain for gram negative bacteria, researchers demonstrated
the presence of a type of bacteria that became known as Rhizobium
(Figure 4). In addition, structural analysis revealed that plant vascular
tissue grew from the nodules to the root vasculature.
The presence of bacteria was demonstrated by numerous researchers
in many, but not all, legumes; and the general conclusion was reached
that these bacteria were associated with most legumes and performed
some function. Researchers suggested that these bacteria were symbioti
cally associated with the plants and that they were responsible for the
nitrogen fixation observed in Seneratne and Hardasons experiment.
Researchers isolated rhizobia and performed experiments on seed
lings inoculated with and grown without the bacteria. Douglas Beck, an
agricultural researcher, set out to test responses of the legume chickpea
(Cicer arietinum) to growing in semi-arid agricultural fields and how
Rhizobium affected chickpea growth. Beck performed both greenhouse
and field experiments. Becks greenhouse experiment tested the effec
tiveness of rhizobia on growth of the plants and nitrogen content in
comparison to growth under conditions of high nitrogen but no rhizo
bia (Figure 5).
He used a nitrogen-free hydroponic gravel system, which contained
gravel and a mineral solution to grow the plants. All materials were steril
ized to kill microbes. The mineral solution contained phosphorus, potas
sium, sulfur, magnesium, calcium, and several nutrients. The solution was
dripped at a slow but constant rate into all pots.
35
nitrogen content of shoots (mg/plant)
30
25
20
15
10
0
rhizobia high N control
treatment
Figure 5 Nitrogen content of chickpea shoots grown hydroponically

with rhizobia and no nitrogen or without rhizobia and high nitrogen.
Data averaged over eight chickpea varieties.
Source: From Beck, 1992, Table 2.
Prior to planting, the outer surface of seeds were sterilized to kill

any rhizobia. Seeds were planted one per pot and inoculated with a rhi
zobial culture. Control pots were not inoculated. Two control treat
ments received one of two solutions that contained a low and high
concentration of nitrogen in the form of nitrate. All plants were harvested
48 days after planting, when they began to flower. Nodulation of roots was
evaluated; all inoculated plants had nodules. Aboveground plant parts were
harvested and dried. Dried material was ground up and analyzed for nitro
gen content using the same technique that Seneratne and Hardason used.
Beck performed another experiment to determine how chickpeas grew
under actual field conditions. Prior to planting chickpea, the scientist ana
lyzed the nitrogen and rhizobia contents of the soil. He found a combined
nitrate and ammonium concentration of 9 mg N/kg. He also found small
numbers of rhizobia (130 viable rhizobia per gram of soil) that were able to
colonize chickpea. Beck added phosphate fertilizer to the field plots. Rhi
zobia plots were fertilized with 20 kg N/ha and inoculated with an average
of 106 rhizobia per chickpea seed, low nitrogen control plots were fertilized
with 20 kg N/ha, and high nitrogen control plots were fertilized twice with
60 kg N/ha. In a portion of treatment plots, Beck set aside a small central
area that received the nitrogen fertilizer with the 15N isotope.
Plant and nodule samples were taken from several plants on each plot
during flowering. Detached nodules were dried and weighed (Figure 6A).
At the end of the experiment, Beck harvested all of the plants in each plot
and determined the final aboveground dry mass per plot (Figure 6B).
He sampled the dried harvested plants for nitrogen (Figure 6C). Several
plants were harvested from the small area fertilized with 15N nitrogen
fertilizer and analyzed for the 15N:14N ratio as Seneratne and Hardason
had done. From this Beck was able to determine the proportion of nitro
gen in the plants that had come from nitrogen fixation (Figure 6D).
Rhizobia colonize legume roots and cause plants to produce nodules.
The nodules are actually made up of plant tissue that grows differently
than other root tissue in response to chemical signals released by the rhi
zobia. The bacteria live in very specific locations within cells, and there
is a vascular system connection between the main root and the nodules.
This regular pattern is good evidence that legumes and rhizobia have an
evolved association with each other.
nodule dry mass per plant aboveground dry mass

400 6
5
metric tons/hectare
300
4
mg/plant
200 3
2
100
1
0 0
A low N high N rhizobia B low N high N rhizobia
total nitrogen per plot total nitrogen fixation per plot
100 100
80 80
kg/hectare
kg/hectare
60 60
40 40
20 20
nd
0 0
C low N high N rhizobia D low N high N rhizobia
Figure 6 Response of chickpeas to two fertilizer conditions or

rhizobia inoculation. A, Mass of nodules per plant sampled during
flowering. B, Aboveground dry mass of harvested plots. C, Total
nitrogen of harvested plots. D, Total nitrogen fixed on harvested
plots; not determined (nd) for high nitrogen plots.
Source: From Beck, 1992, Tables 3 and 4.
The experiments by Beck showed that in the presence of rhizobia

chickpea plants can grow. If plants were grown hydroponically, where
all nutrients can be controlled, the absence of nitrogen should have
prevented the plants from growing. Beck did not include a no-nitrogen,
no-rhizobia treatment for just that reasonthe plants would have died.
The presence of rhizobia allowed plants to obtain nitrogen from the
nitrogen fixation ability of the bacteria, and they gained almost as much
nitrogen as the plants grown without rhizobia and with high nitrate. This
was an accurate indication, then, of nitrogen fixation.
It was not possible to exclude rhizobia from the field trials, and Beck
showed that preexisting rhizobia colonized plants in the low and high
nitrogen plots but to a much lesser degree than plots where he added
rhizobia. Plots with rhizobia did as well as plots with high nitrogen and
slightly better than plots with low nitrogen in both accumulation of dry
mass and total nitrogen. Growth of rhizobia is facilitated by the large inoc
ulation provided by the researcher and that allowed plants to be colonized
by more bacteria, grow more nodules, and fix more nitrogen than plants
in plots that were given the same level of fertilizer (low) and no rhizobia.
Nitrogen fixation appears to be related to nodule mass. In other
experiments, legumes with rhizobia gained more nitrogen when culti
vated in nitrogen-free soil than in soil containing nitrogen. The presence
of nitrates in the soil appeared to inhibit the growth of nodules. High
levels of nitrogen in the form of nitrate in Becks experiment might have
prevented nodules from growing simply because the plant does not need
the extra help from rhizobia. If the plants need nitrogen fixed for them,
they house the bacteria, but when nitrogen in the form of nitrate is in
ready supply, rhizobial growth is somehow inhibited or blocked. This
indicates that the plant might incur a cost to housing high numbers of
rhizobia. It turns out that in this symbiotic relationship, plants provide
the rhizobia with a place to live and energy in the form of organic carbon
compounds. In return, the plant obtains essential nitrogen.
Nitrogen fixation can be carried out by more than just rhizobial bac
teria. Numerous other types of bacteria are also nitrogen-fixers. Micro
organisms that fix nitrogen have enormous effects in ecological systems,
because they are the major source of usable nitrogen to ecological sys
tems. Plants can take up nitrates and some other nitrogen-containing
compounds, and animals can take up nitrogen when eating plants and
other animals.
As shown with data above, the first step in the nitrogen cycle (Figure 7)
can be considered the fixation of atmospheric nitrogen into a form usable
by biological organisms. The nitrogen cycle describes the circulation and
chemical reactions of nitrogen in ecological systems. Populations of single-
celled organisms, living in the soil, in aquatic habitats, and in symbi
otic relationship with multicellular organisms are critical in this regard.
This cycle is one of several nutrient cycles found in ecological systems.
Nutrient cycles are all the processes by which nutrients change chemical
form and are transferred from one part of an ecological system to another.
Nitrogen, as one important nutrient, can be traced from the atmosphere
nitrogen in
atomosphere (N2)
plants
assimilation
denitrifying
nitrogen-fixing decomposers bacteria
bacteria in
root nodules nitrates (NO3)
of legumes
nitrifying
aerobic and anaeobic
bacteria and bacteria
fungi
decomposition nitrification
ammonium nitrites
(NH4+) (NO2)
nitrogen-fixing nitrifying
soil bacteria bacteria
Figure 7 The nitrogen cycle showing compartments that contain

nitrogen and the form of nitrogen in each compartment.
Source: Adapted from http://www.epa.gov/ maia/html/nitrogen.html (public domain image).
to Rhizobium bacteria that convert it to ammonia and then incorporate it

into their amino acids and provide it to legumes.
That nitrogen is then assimilated by animals and humans that con
sume the legumes or plants that grow in the soil after the legumes
die and decompose. There is thus a beneficial effect of legumes on
other plants. Now two more steps in the nitrogen cycle are known:
assimilation and decomposition. Assimilation results in production
of organic forms of nitrogen, including proteins and DNA, and can
also be considered the incorporation or conversion of nutrients into
organisms following absorption. Decomposition is the decay into con
stituent parts by physical, chemical, or biological processes, which is a
reversal of the process and usually results in formation of ammonium
or ammonia.
220
cummulative nitrite (mg nitrite/day/100 ml)

200
180
160
140
120
100
80
60
40
20
0
0 4 8 12 16 20 24 28
day
Figure 8 Accumulation of nitrite in bacterial cultures provided with

ammonium sulfate, average +/ 1 standard error is shown.
Source: From Bonazzi, 1918, Tables 2, 3, and 4.
If assimilation by plants requires nitrate, and nitrogen fixation and

decomposition produce ammonium, there ought to be other steps of the
cycle involved in converting ammonium to nitrate. Around the same
time that agricultural scientists were beginning to study legumes and
rhizobia, microbiologists were examining the soil for the factors that
oxidized ammonium to nitrite and nitrate. Augusto Bonazzi used culture
techniques to successfully isolate a soil bacterium. He determined the set
of conditions under which vigorous growth of this bacterium resulted
oxygen, gentle agitation and a medium of water, ammonium sulfate and
various salts. In addition, Bonazzi added clumps of soil that had been
baked in an oven at 700o C.
Bonazzi measured nitrite at intervals over the growth of replicate
cultures (Figure 8). When sampling for nitrite, the scientist took 5 mL
from a culture with a sterile pipette, diluted the sample in a volu
metric flask, and measured nitrite twice for each sample. The results
are expressed as milligrams of nitrogen oxidized to nitrite per day in
100 mL of culture.
The bacteria in these cultures appear to be converting ammonium to

nitrite. These cultures had been grown in the lab for many generations,
and the attempt was made to keep them free of other bacteria. In cul
tures of bacteria that do not oxidize ammonium, no nitrite accumulates.
Bonazzi did not show this, nor did he conduct a no-bacteria control to
show that nitrite accumulates only in cultures with these bacteria. How
ever, this experiment and others performed by other scientists on these
bacteria demonstrated clearly that they were converting ammonium to
nitrite. It turns out that Bonazzi had isolated a species of Nitrosomonas
bacteria. The oxidation of ammonium into nitrite is performed by bac
teria that belong to the two genera Nitrosomonas and Nitrosococcus, as
well as other species.
Nitrite is often not found in significant quantities in the soil, and
part of the reason is that there is another step in the nitrogen cycle, the
oxidation of nitrite to nitrate, called nitrification (Figure 7). Nitrifica
tion is the conversion of ammonium to nitrite and nitrite to nitrate.
Other researchers working on soil bacteria, using methods very similar
to Bonazzis, discovered that bacteria of the genus Nitrobacter convert
nitrite to nitrate. Although plants without symbiotic bacteria can take
up a variety of forms of nitrogen in the assimilation stage, the preferred
form seems to be nitrate. These two steps of the nitrogen cycle, the con
version of ammonium to nitrite and nitrite to nitrate, evolved as part of
the metabolism of these bacteria. The conversions transduce energy that
is coupled to adenine triphosphate (ATP) synthesis. The populations of
bacteria that utilize these steps in their metabolism are not altruistic;
they benefit other species only in the context of performing an activity
for themselves. This is an emergent property of ecological systems, as
is the entire nitrogen cycle. Nitrogen cycles in ecological systems as a
result of the ecology of a variety of organisms, including many essential
unicellular species.
One final step in the nitrogen cycle is also a result of bacteria metabo
lizing a nitrogen compound. Denitrification is performed by microor
ganisms that convert nitrate or nitrite in the soil and aquatic habitats to
atmospheric nitrogen or nitrous oxide. Denitrification is a microbially
facilitated process of nitrate reduction that produces molecular nitrogen.
This usually occurs during the anaerobic breakdown of organic matter,
where nitrate is used in place of oxygen as an electron acceptor in the

oxidation of organic matter and may involve several steps and species of
bacteria. With this final step, the nitrogen cycle is complete, as denitri
fication ultimately produces molecular nitrogen (N2), which is released
back into the atmosphere. As with the reactions involved in nitrification,
the bacteria perform them as part of their metabolism with the end result
being a profound effect on ecological systems and an emergent property
of those systems.
Ethical, Legal, Social Implications:

There are Positive and Negative Consequences
of Agricultural Practices on Soil Ecosystems
Humans have devised many ways to increase the yield of crops harvested
per acre through the development of agricultural technology. Fertilizers,
pesticides, genetic engineering, tillage, and irrigation have all played a
role in the so-called Green Revolution, which transformed agriculture
beginning in the 1940s. The transformation of agriculture into a more
mechanized industrial practice led to growth of great quantities of agri
cultural products to feed a growing population. One could argue that
the rapid increase of the human population was a result of agricultural
practices developed in the twentieth century, as the human population
grew from an estimated 2 billion people in 1930 to almost 7 billion by
2010. Although the advantages of producing more food to feed humans
are obvious, green revolution techniques can have adverse environmental
effects. Ecological systems in soil can suffer some of these effects.
In the last century, humans developed inorganic fertilizers that can be
produced in mass quantities. These inorganic fertilizers contain nitrogen
fixed as ammonium and nitrate through industrial processes. The indus
trial fixation of nitrogen was one of the most important developments in
modern agriculture, as evidenced by the tremendous gains in productiv
ity experienced in agriculture since the 1940s. It could be argued that
inorganic synthetic fertilizer is essential for meeting global food demands.
Synthetic fertilizers enabled farmers to convert infertile lands into fertile
fields and to grow crops in the same soil year after year without waiting
for nutrients to regenerate naturally.
The downsides to use of industrialized produced nitrogen fertilizers

include leaching and erosion of excess nitrate from soil during rains,
which can cause algal blooms in aquatic ecological systems. Too much
nitrogen in the soil can actually be a bad thing for growth of plants, and
it can lead to yellowing of leaves, slow growth, and spindly stems. When
nitrogen is added to soils where legumes are grown, rhizobial bacteria are
taken up in lower quantities by those legumes. They simply do not need
the symbiotic bacteria to fix atmospheric nitrogen if it is already available
as nitrate or ammonium.
Another important technological development has been in the area
of chemical pest control. Agricultural ecosystems may seem very simple,
especially aboveground. One to several species of plants are sown and
grown by humans in one field, although other plants may also grow. These
plants are undesirable; we call them weeds. The plant community sup
ports several to many species of animals, some of which are pests on the
plants we grow. At the soil surface, and a few centimeters belowground,
there is a diversity of organisms that play roles as pests, as predators, and
in nutrient cycling. The monocultures typically used in intensive agricul
ture lead to increases in the number of pests, which are usually controlled
with pesticides. The chemicals developed to control the weeds and pests
of our crops have been important in controlling damage done by these
populations. Chemical pesticides have allowed farmers to grow crops and
raise livestock in high densities with higher yields and less damage to
crops and livestock. Being able to grow more food on less land averts the
need to cultivate more land for a growing human population. More land
converted to crops for humans means less land for other species.
However, use of pesticides has contributed greatly to environmen
tal pollution. Many pesticides have effects on species that are not pests,
including beneficial predators and humans. There are pesticides that
mimic animal hormones, that have carcinogenic and neurotoxicologic
effects, and that disrupt enzyme function in a variety of animals. Many
of the affected organisms live in the soil beneath the crops. Pesticides
sprayed on a crop often drift, through the air and water, to natural habi
tats, disrupting those ecological systems.
Fertilizers and pesticides are often applied with heavy machinery, and
this machinery is also involved in harvesting crops and tilling the soil.
Tilling, or plowing the soil mixes, loosens, and aerates the soil, allow
ing for deeper penetration of roots. As a result of all this machinery, the
soil underfoot may suffer from compaction, which means that the spaces
between soil particles are lost and soils lose their ability to hold air and
water. Healthy soils must have air and water for the communities of organ
isms living in soils. It is difficult for plant roots to grow and earthworms
to burrow in heavily compacted soils. In addition, agricultural machinery
burns fossil fuels, and this can contribute to global climate change and
air pollution. Tilling the soil can have detrimental effects because the act
of plowing and loosening the soil may facilitate erosion and disrupt com
munities of organisms living in the soil. Erosion, as mentioned, leads to
loss of nutrients and movement of pesticides.
Other potential adverse effects on soil ecological systems include
desertification and salinization. Desertification is the deterioration of
land in arid habitats due to loss of vegetation and soil moisture caused
primarily by human activities, including overgrazing, over drafting of
groundwater, and diversion of water from rivers. Salinization is the accu
mulation of salts in soils caused by irrigation and subsequent evaporation
of water. Freshwater contains small quantities of salts, and evaporation
removes the water but not the salts, which build up. Most soil organisms
and many plants are not adapted to living in these very salty conditions.
Although the intensive Green Revolution agricultural techniques
clearly have benefits, there are also drawbacks. Intensive agriculture has
become associated with decreased soil quality around the world, and
there is increased concern over the effects of fertilizers and pesticides on
the environment. As the human population and food demand increases,
agriculture responds. How we respond and what we do as a society will
depend on our values and our consideration of sustainability. If current
agricultural practices produce enough food to feed humanity but cause
long-term losses in soil quality, then these practices are not sustainable
and hurt the ability of future generations to produce enough food. The
degradation of soils ultimately affects our ability to feed humans. If we
decide we are only concerned with feeding the current population, then
future soil health is not an issue. If we are concerned about future genera
tions, we could still continue as we are and put our trust in those future
humans to develop new techniques to deal with the problems of lowered
soil quality. How future humans respond and what technologies they
develop are unpredictable from our vantage point. But another response
would be to begin practicing techniques that are more sustainable in the
long-term.
Bibliography
Allen ON, Allen EK: Response of the peanut plant to inoculation with
rhizobia, with special reference to morphological development of the
nodules, Botanical Gazette 102(1):121142, 1940.
Beck DB: Yield and nitrogen fixation of chickpea cultivars in response
to inoculation with selected rhizobial strains, Agronomy Journal 84:
510516, 1992.
Bonazzi A: On nitrification: II. Intensive nitrite formation in solution,
J Bacteriol 4(1):4360, 1918.
Fred EB, Baldwin IL, McCoy, E: Root nodule bacteria and leguminous
plants, University of Wisconsin Digital Collections (website): http://
digicoll.library.wisc.edu/HistSciTech/subcollections/RootNodule
About.html. Accessed July 13, 2014.
Lebert M, Bken H: Soil compaction. The Encyclopedia of Earth
(website): http://www.eoearth.org/article/Soil_compaction, Accessed
July 13, 2014.
Seneratne R, Hardason G: Estimation of residual N effect of fababean
and pea on two succeeding cereals using 15N methodology, Plant Soil
110:8189, 1988.
Taubert PHW: Leguminosae. In Engelmann, editor: Natrliche
Pflanzenfamilien, Vol. III, 1891.
Ward JR, Ethridge MM, Brouwers EM: Investigating the environmental
effects of agriculture practices on natural resources, US Geological
Survey Fact Sheet 2007-3001 (online PDF): http://pubs.usgs.gov/
fs/2007/3001/pdf/508FS2007_3001.pdf, Accessed July 13. 2014.
CHAPTER 3
Certain Phytoplankton can

Produce a Red Tide
In 1990, six fishermen nearly died from eating mussels during a fish
ing trip on Georges Bank, an offshore fishing area east of Cape Cod,
Massachusetts. The mussels were inadvertently caught in their nets,
and they decided to steam them for dinner. The fishermen very quickly
became incapacitated and showed signs of paralysis. The Captain, who
had joined the meal late, sent an SOS to the Coast Guard when he saw
what was happening to his crew, prior to becoming paralyzed himself.
After being rescued by the Coast Guard, the fishermen, whose lungs
were paralyzed, were kept alive with ventilators. Thankfully, all the fish
ermen survived. The paralysis of the fishermen was hypothesized to have
been caused by a massive algal bloom, or red tide, and in response the
clam and mussel fisheries on Georges Bank were closed to fishermen.
An algal bloom is the rapid growth of a large population of algae, and
a red tide is an algal bloom caused by dinoflagellates that color coastal
waters reddish.
In the first two chapters of this book, several important roles that
unicellular organisms can play in ecological systems were considered.
Free-floating microscopic unicellular organisms, composed of protists
and bacteria, and collectively known as plankton, occur near the surface
of the oceans. The photosynthetic species are phytoplankton. Popu
lations of algae grow in the ocean just as other species of unicellular
organisms grow, and very large populations, the algal blooms or red tides,
often occur in marine coastal zones. In this chapter, the factors that lead
to large populations of these unicellular organisms and how they affect
ecological systems will be explored.
Jing Zhang studied some of the factors that may contribute to algal
blooms in the Yellow Sea. He used data collected on nutrients between
1988 and 1993 from two monitoring stations on the east coast of China.
Station 1 was located close to a major urban area, and Station 2 was
located on a remote peninsula surrounded by the Yellow Sea on three
sides and agricultural areas on the landward side. Individual precipitation
events may last for hours to several days with rainfall ranging from less
than 1 mm to 200 mm. Precipitation between May and August accounts
for about 70% to 80% of annual rainfall and is higher at Station 2 due to
the wind patterns. A single rain event in this wet season may contribute
up to 30% of annual rainfall in this region.
Researchers working at the stations measured the amount of precipi
tation and the nutrient composition of wet deposition of coastal waters
and of water entering the ocean from rivers. Wet deposition is the process
by which aerosol particles are removed from the atmosphere by water
droplets. The researchers determined concentrations of nitrate (NO3),
nitrite (NO2), ammonium (NH4+), phosphate (PO43), and dissolved
silicon (SiO2) using standard methods (Figure 9A).
Once the precipitation amount was determined, that liquid was sam
pled for nutrients. The scientists used the same techniques to measure
nutrients in ocean water from monthly water samples. The concentra
tions in river water and precipitation were also used to determine the
amount (not the concentration) of nutrients delivered to the ocean via
either precipitation or river flow, based on the amount of liquid input
into the ocean each month. Zhang used these data to calculate for each
nutrient the average contribution to the Yellow Sea from precipitation
and river water (Figure 9B).
Zhang found spatial, temporal and source differences in deposition
of nutrients. There were station differences in wet deposition, which he
concluded were due to the proximity of station 1 to a major urban area.
Emissions from factories, automobiles, and power plants can contain
nutrient compounds, and several nutrients were found in higher con
centrations in wet deposition collected at station 1. More phosphate
and ammonium enters the ocean from deposition than from freshwater
river flows, although the river is a significant source of dissolved silicon
dioxide.
Certain Phytoplankton can Produce a Red Tide 29
14 nutrient concentrations
12 = station 1 average
concentration (mmol/kg:
= station 2 average
NH4 values 3 101)
10 = Yellow Sea maximum
0
te
te
ox on
at
tra
tri
iu
di ilic
e
ph
on
ni
id
ni
s
os
m
am
ph
A
6 nutrient inputs to the Yellow Sea
= precipitation
5 = river
nutrient input (109 mol/yr)
0
te
te
te
ox on
tra
tri
iu
ha
di ilic
e
on
ni
id
p
ni
s
os
m
am
ph
Figure 9 Nutrient concentrations of water sources (A) and nutrient

inputs into coastal Yellow Sea habitats (B).
Source: From Zhang, 1994, Tables 1 and 2.
Finally, the researchers at the stations recorded the dates, locations,

and species of algal blooms, which Zhang used in his analysis. Zhang
plotted the percentage of total toxic algal blooms against the percentage
of total deposition of each nutrient (dissolved inorganic nitrogen [DIN],
phosphate, and silicon dioxide) that occurred in a particular month
events (blooms) or deposition (nutrients) 35
= toxic bloom events (%)

30
= inorganic nitrogen (%)
= phosphate (%)
percentage of annual total
25 = silicon dioxide (%)
20
15
10
0
Apr May Jun Jul Aug Sep Oct Nov
month
Figure 10 Percentages of total toxic algal bloom events and total

annual deposition for nutrients that occurred in each month, averaged
over 6 years (19881993). Blooms only occurred between April and
November.
Source: Data from Zhang, 1994, Figure 5.
(Figure 10). These blooms are caused by algae that release chemicals toxic
to other organisms. For this comparison, he combined nitrate, nitrite,
and ammonium to calculate the total DIN.
For the most part, higher deposition of nutrients in summer months
leads to a higher percentage of annual algal blooms occurring in those
months. Twenty percent of all toxic bloom events occur in July, which is
the month with the highest percentage of annual deposition of all nutri
ents tested. Higher deposition rates are due to higher precipitation during
the April to November wet season. Nutrients that enter the water during a
rain event may be taken up quickly by phytoplankton, causing the rapid
population growth characteristic of a bloom.
Zhang also described the trend in the number of algal blooms in
Chinese coastal waters over time, recorded since 1970. Over a 22 year
period the number of toxic algal blooms per year increased dramatically,
from near zero in 1971 to over 40 per year in the early 1990s. More
recent data suggest that the number continues to rise to 5080 per year,
depending upon the year.
Beginning in the late 1960s and continuing to today, Chinas

economy has been growing at a very high rate. Along with the growing
economy, there has been growth in the number of power plants, factories,
and automobiles. More economic growth often means more emissions
of potential pollutants. Even though the chemicals that Zhang studied
are nutrients to plants, too much of anything can pollute and lead to
adverse ecological effects. The increases in deposition due to industrial
ization is a concernas the data show, toxic algal blooms have increased
in the Yellow Sea during the period of rapid economic growth. Zhang
did not demonstrate a direct link between economic growth, nutrient
inputs, and toxic algal blooms; but the correlation does generate some
concern about the factors that cause algal blooms and how they might
change as a consequence of human activities.
Incidences of red tides of toxic dinoflagellates belonging to the
Alexandrium genus have been monitored by scientists worldwide in an
effort to determine the cause of such blooms. Although there are known
correlations of blooms with nutrient inputs, as Zhang found, the specific
factors causing rapid population growth of Alexandrium minutum was
investigated by Jean-Francois Maguer and his colleagues. This dinoflagel
late appeared in estuaries off the northwest coast of France in the late
1980s. A bloom recurs every year in the Penze estuary, and the scien
tists had collected data for 3 years on several environmental parameters
(Figure 11).
The predictability of blooms, usually in June, gave the scientists the
opportunity to study one bloom intensively, which they did in the third
year of data collection. The researchers set up a sampling regime to collect
data before, during, and after the predicted bloom.
At each sampling, the scientists collected data from an area where salin
ity was above 20 parts per thousand (ppt), because blooms of this spe
cies did not occur in waters of low salinity. The scientists brought water
samples to the laboratory, where they counted the number of algal cells
and determined the concentrations of nitrate, ammonium, and phosphate.
Phytoplankton cells were counted under the microscope, with density
calculated as number of cells per unit volume. At the peak of the bloom,
A. minutum made up about 60% of the cells counted (Figure 12). At
the end of the A. minutum bloom, a bloom by another species occurred.
35 35
30 30
cells (3 106 L1)
max density of
25 25
20 20
15 15
10 10
5 5
0 0
16 17 18 19 20 26.0 26.5 27.0 27.5 28.0
A temperature (C) B salinity (ppt)
35
max density of cells
30
25
(3 106 L1)
20
15
10
5
0
150 200 250 300 350 400 450 500 550
C
nitrate (mmol/L)
35 35
30 30
cells (3 106 L1)
max density of
25 25
20 20
15 15
10 10
5 5
0 0
0 2 4 6 8 10 12 14 1.4 1.6 1.8 2.0 2.2 2.4 2.6 2.8 3.0
D ammonium (mmol/L) E phosphate (mmol/L)
Figure 11 Maximum bloom of A. minutum over 3 years plotted

against environmental parameters measured during each years bloom
in an estuary off the coast of France. A, Temperature; B, salinity;
C, nitrate; D, ammonium; E, phosphate.
Source: From Maguer et al., 2004, Table 1.
Maguer and his colleagues measured nutrient concentrations in the water

and the rate of uptake of nitrate, ammonium, and phosphate in samples
of water that contained A. minutum cells with the idea that uptake would
be high when the population was rapidly growing. They did this by add
ing radioactively labeled versions of the nutrients into sample bottles,
which were then sealed and placed in the estuary in the middle of the day.
At the end of the incubation period, the water was filtered. Once that was
done, the scientists determined uptake of nutrients during the incubation
period.
35
number of cells (3 106 L1) 30
25
20
15
10
0
ay
ay
l
Ju
Ju
Ju
Ju
Ju
Ju
Ju
Ju
Ju
M
04
02
06
10
14
18
22
26
30
25
29
date
Figure 12 Changes in cell densities of A. minutum during the algal

bloom in an estuary off the coast of France in 1999.
Source: From Maguer et al., 2004, Figure 1.
By studying a recurring bloom in one estuary off the coast of France,

Maguer and his colleagues were able to learn about the specific require
ments of one algal species and what caused it to grow to very large popu
lation sizes in a short time. In the bloom they studied, the population
grew from a few thousand cells per liter on June 9th to over 33,000,000
cells per liter on June 22nd. By the end of June, densities had declined
back to less than 50,000 cells per liter. Both temperature and salinity had
an impact on the size of a bloom in any given year, although it is difficult
to determine which factor may be more important in determining size of
the bloom. Salinity that is too high or temperatures that are too low are
correlated with less dense algal blooms. High ammonium concentrations
are also correlated with less dense blooms, although there seems to be no
correlation with nitrate or phosphate concentrations.
In the bloom examined over time, nutrient concentrations declined,
especially when the bloom was at its peak. Nitrate, although it declined,
was still present in the water at very high concentrations. Uptake rates
were highest for ammonium prior to the bloom and for nitrate during
the bloom. This is possibly due to loss of ammonium from the water;
the growing algal populations essentially stripped the ammonium from

the water and then had to switch to nitrate as another source of nitrogen.
High ambient concentrations and uptake rates of nitrate during the peak
of the bloom indicated to Maguer and his colleagues that it is the sup
ply of nitrate that sustains the bloom. Although phosphate uptake also
peaked with the growing bloom, phosphate concentrations did not drop
to near zero as they did with ammonium. If they had, there would have
been no substitute nutrient, and growth of the bloom would have likely
been stopped. Although excessive nutrients could be responsible for an
algal bloom, the researchers noted that blooms never occur in low salin
ity waters or waters cooler than 16o C. They concluded that the proper
temperature and salinity conditions are required to initiate the bloom.
The scientists also measured daily water surface irradiance, which is
a measure of the amount of light energy entering the water, and photo
synthetically active radiation (PAR), using a probe that was immersed
1 meter deep. The presence of high light levels for several days prior to
the beginning of the bloom allowed for high rates of photosynthesis and
consequently fast growth of the algal population. Along with the nutri
ent conditions of the water, the conditions were right for an algal bloom.
The algal bloom lasted for only a couple of weeks. The researchers
observed that the amount of photosynthetically active light at 1 meter
depth is very low during peak algal bloom. A PAR of about 10% is nec
essary to maintain dinoflagellate growth, and with PAR below that for
several days, the population may have grown so much as to cause condi
tions that were unsuitable for continued growth. Phosphate could have
also caused the decline, because concentrations were never very high to
begin with, and there may not have been enough to sustain the massive
population at peak bloom. Not only do conditions have to be right to
cause an algal bloom, the bloom itself changes the conditions in the envi
ronment and that leads to a decline in the population causing the bloom.
The logistic model of growth, mentioned in Chapter 1, can be used
to represent what happens when a population exceeds the capacity of
its resources. The algae population skyrockets during a bloom, and then
it typically crashes back down to nearly zero until conditions are right
for another bloom. A simple way to account for limited resources is to
multiply the increase in the population by a factor that is close to 1 when
the population is small but gets closer to 0 as the population increases

toward its theoretical limit, or carrying capacity. Carrying capacity is the
maximum, equilibrium number of organisms of a particular species that
can be supported indefinitely in a given environment. If K is the carrying
capacity, then the factor (1Pt/K ) has these characteristics. The resulting
equation for this so-called logistic model is Pt+1 = Pt + r Pt (1Pt/K ).
The increase in population under this model is about the same as that
for exponential growth when Pt is small. However, when Pt is close to K,
the increase in population is small relative to Pt. For growth rate values
of r near 1, the logistic model is a good match to the S-shaped curves
described in Chapter 1, with a log phase and a stationary phase. When r is
closer to 3, growth rate is exceedingly high, and this rapid growth causes
the population to shoot past carrying capacity, which is then followed by
population collapse, just as observed in the algal bloom.
As with the study in the Yellow Sea, researchers linked algal blooms
to the presence of nutrients. Maguer and his colleagues noted that heavy
application of nitrogen-based fertilizers in agricultural areas leads to wash
ing of nutrients into rivers, estuaries, and coastal waters. These inputs,
different from sources correlated with blooms in the Yellow Sea, are cor
related with increased incidences of algal blooms. Researchers studying
algal blooms around the world have concluded that better management
of fertilizer use and reduction of emissions of nutrient-containing pol
lution is necessary to reduce toxic algal blooms. Keep in mind that the
conditions that cause blooms may vary depending upon the species.
Phytoplankton form the base of food webs, upon which nearly all
marine organisms depend, and rapid population growth may have effects
on other species in ecological systems. Because this chapter examines
cells at the ecological system level, it is appropriate to ask not only what
causes red tides but what effects they have on ecological systems. This is
where we return to the story of the fishermen poisoned by eating mussels.
How is it that the mussels poisoned the fishermen? Are there effects of
dinoflagellate algal blooms on other organisms?
Anita Sievers performed experiments to test the effects of high densities
of two species of dinoflagellates on a variety of marine creatures from dif
ferent taxonomic groups. She grew single species cultures of Alexandrium
monilatum and Gymnodinium breve, both of which are known to bloom
during periods of mass mortality of other organisms. Notice that one of

the species belonged to the same genus as the dinoflagellate studied by
Maguer and colleagues. The cultures were grown in constant conditions
in large containers. Sievers determined the density of cells in cultures as
they grew. Because of previous work on toxicity of these species to fish, the
scientist chose to work with densities of 0.7, 1.0, and 1.2 million cells per
liter for A. monilatum, and 5.0 and 9.9 million cells per liter for G. breve.
When cultures reached the desired densities, Sievers collected some of the
culture and froze it at 18o C. She hypothesized that when cells in blooms
died because they were in such high densities, the cells broke apart and
released toxin into the environment. Freezing the cells in her experiment
ensured maximum disruption.
Sievers exposed seven different animal species to these cell cultures: a
minnow, a barnacle, a mud crab, a grass shrimp, a marine worm, and two
types of shellfish (an oyster and a mussel). Ten animals of each species
were tested at a particular concentration for 48 hours (Figure 13). Not
all concentrations were tested with each species. Each test was conducted
with the ten animals exposed to 1 liter of test culture. The control treat
ment was to hold ten animals in similar conditions, but without dinofla
gellate toxins, for 48 hours.
The hypothesis that toxin comes from dinoflagellates is supported
by the data, but the dinoflagellates have effects that differ among some
of the species of marine animals tested. The fish and the worm were
susceptible to toxins from both dinoflagellate species. The grass shrimp,
an arthropod, was mildly affected by toxins from both algae. The bar
nacle and the mud crab, also arthropods, were unaffected by the toxins.
The shellfish were strongly affected by the toxin from A. monilatum.
When dinoflagellates are in low density in the ocean, mass mortality
of populations of marine animals is not observed, indicating that the
toxin, even if it is produced by dinoflagellates when at low density,
is either not being released or the concentration is too low to do any
harm. During and right after a bloom, there are high densities of dino
flagellates; and in large populations, mortality may be high. When large
numbers of cells die and break apart, high concentrations of toxin may
be released, exerting differential effects on coastal marine species and
ecological systems.
100
= control
mortality after 48 hours exposure = A.m. 0.7
80 = A.m. 1.0
= A.m. 5.0
= A.m. 9.9
60
40
20
nd
nd
nd
nd
0
w
le
ab
er
l
se
rim
no
ac
or
st
cr
us
oy
w
in
rn
sh
ud
m
m
ba
s
m
as
gr
Figure 13 Percentage mortality of test populations of different species

in response to 48 hour exposure to cells of one of two dinoflagellate
species at different concentrations. The numbers in the legend (0.7,
1.0, 5.0, and 9.9) are concentrations of cell cultures 3 106. A.m.
- Alexandrium monilatum; G.b. - Gymnodinium breve; nd - not
determined (all other absent bars are 0 values).
Source: From Sievers, 1969, Figures 1-8.
Blooms of some species have been associated with poisoning shellfish,

and occurrence of one type of bloom, caused by Alexandrium species and
called paralytic shellfish poisoning (PSP), have been monitored over time
(Figure 14). It is thought that a bloom of some Alexandrium species is
what caused paralysis in the fishermen from our earlier story. Mussels
and oysters are susceptible to toxin from Alexandrium; and during the
early part of a bloom, mussels ingest toxin from the surrounding water.
If they are caught and consumed by humans before they themselves con
sume enough toxin to be killed, the humans that eat enough shellfish may
exhibit signs of poisoning, and humans have been known to die from
eating contaminated shellfish.
In ecological systems, rapid growth of one species often has impacts
on other species, and this is no exception, because A. minutum and other
algae create blooms that are toxic to other organisms.
40
# of paralytic shellfish poisoning events
= through 1970
= 19712006
30
20
10
0
a
pe
ia
lia
ic
ic
ric
As
ra
ro
er
er
Af
st
Eu
m
Am
Au
.A
S.
N
Figure 14 Documented occurrences of PSP associated with algal

blooms through 1970 and 1971 to 2000.
Source: Data from http://www.whoi.edu/redtide/ page.do?pid=18103
In summary, blooms of toxic algae can have large impacts on species

in marine ecological systems. Poisoning of shellfish can lead to adverse
health effects on organisms that feed on shellfish, including humans.
Marine ecological systems around the world annually experience blooms
of dinoflagellates, some of which are responsible for PSP. To protect eco
logical systems and human health, scientists monitor red tides and natural
shellfish populations.
Toxic algal blooms are caused by Alexandrium species, but other spe
cies of algae are also known to have toxic effects. The blooms resulting
from these species may be red, brown, or otherwise colored, so the term
red tide has been largely replaced by the term harmful algal bloom
(HAB). The ecological effects of these different species are variable.
Scientists have concluded that increased inputs of nutrients into water
ways from human activities have caused changes in coastal marine eco
logical systems, and these inputs are often associated with the presence
of toxic algal blooms. Increases in nutrient input are leading to increases
in frequency of blooms throughout the worlds coastal ocean habitats,
which often cause negative effects, including high rates of mortality, on
populations of other organisms through the production of toxins. Blooms

of algae can also cause depletion of oxygen from shallow coastal waters
or physical damage to fish gills, leading to asphyxiation, and effects on
humans and our economic activity.
Ethical, Legal, Social Implications:

Seeding the Oceans with Iron to Increase Productivity
and Create a Carbon Sink has Consequences
One of the major environmental issues that humanity faces is global
climate change. A 2007 report of the Intergovernmental Panel on
Climate Change (IPCC), which reviews all peer-reviewed literature on
climate change and its causes and mitigation, concluded that the release
of greenhouse gases by humans, especially carbon dioxide (CO2), is play
ing a significant role in changing climate. Mitigation of climate change
most often deals with how we can either reduce global CO2 emissions or
extract CO2 from the atmosphere.
One hypothesis that has been experimentally tested several times
in the open ocean is the iron hypothesis, put forward by Dr. John
Martin in the 1980s. There were several observations Martin used to
construct this hypothesis. First, it was known that phytoplankton, in
the course of photosynthesizing, drew down millions of tons of CO2
from the atmosphere each year. Second, phytoplankton may be eaten by
zooplankton or may sink to the bottom of the ocean when they die. In
the first instance, the CO2 absorbed by the phytoplankton is released by
the zooplankton through the process of respiration, often ending up back
in the atmosphere. In the second, the CO2 is transported to the bottom
of the ocean, where it may become trapped for millions of years in the
sediments. The CO2 is sequestered. The third observation is that there
are areas of the ocean that are high in nitrogen and phosphorus, but
low in phytoplankton density, suggesting some other nutrient is limiting
their growth.
Martin speculated that iron, a micronutrient essential for phytoplank
ton in minute amounts, was deficient in the open ocean, because the only
source of it was from dust blown from land to the ocean. Fertilizing these
areas with iron could spur phytoplankton growth and thus remove about
15% of CO2 that humans annually add to the atmosphere, according to

proponents.
The iron hypothesis has been controversial for several reasons.
Researchers have argued that it is an inefficient way of capturing and
storing carbon. Environmentalists have argued that the full ramifications
of large scale iron fertilization on marine ecosystems are unknown. They
also argue that it could inadvertently release other greenhouse gasses (such
as, methane) that are more potent in trapping heat, or that the iron could
stimulate the growth of harmful algae, such as the ones that cause red
tides. Further, we would have to fertilize the ocean every year to maintain
the effect, just like many people fertilize their lawns annually.
The concerns have been great enough that the United Nations
Convention on Biological Diversity (UNCBD) imposed a moratorium
on ocean fertilization by commercial interests, although they allowed
it on small-scale, research expeditions in coastal waters. The UNCBD
awaits results of research and a better understanding of the technology
before lifting the moratorium. Some scientists argue that this restricts
research too severely; for instance, some would perform experiments in
the open ocean and now cannot under the moratorium.
Recently, commercial companies have taken an interest in Martins
hypothesis in order to make money from carbon market, a proposed
mechanism to mitigate global climate change. Commercial emitters of
CO2 will be able to buy and sell carbon credits in a market that works like
a stock exchange. Offsetting carbon emitted somewhere else by allowing
algae to take it up in the ocean is an inexpensive way of making carbon
credits that can be sold on the market.
Since the mid-1990s, scientists around the world have tested the iron
hypothesis by adding iron to the ocean and observing the responses of
phytoplankton. Two recent iron fertilization experiments performed in
the late 2000s, studied both a natural volcanic source of iron that finds its
way into the Southern Ocean and several tons of iron sulfate made from
powder that can be bought to treat lawns. Both experiments spread the
iron compounds over dozens of square kilometers of ocean. They both
found that blooms of phytoplankton occurred almost immediately and
that a large amount of the new biomass sank to the bottom of the ocean
several weeks after the bloom occurred. This finding is different from what
several earlier experiments found, which often found that carbon was
exported down but often not very far. Scientists argue that much more
research is required in order to understand how much iron is needed,
in what form it should be added, and what effects the fertilization has
on communities of plankton in the ocean and on marine food webs. In
assessing the utility of iron fertilization as a tool to mitigate global climate
change and save the planet, we must first understand the basic science.
Bibliography
Gilbert PM, Anderson DM, Gentien P, et al.: The global, complex
phenomena of harmful algal blooms, Oceanography 18(2):130141,
2005.
Maguer J-F, Wafar M, Madec C, et al.: Nitrogen and phosphorus require
ments of an Alexandrium minutum bloom in the Penz Estuary,
France, Limnol Oceanogr 49(4):11081114, 2004.
McGillicuddy DJ Jr, Anderson DM, Solow AR, et al.: Interannual
variability of Alexandrium fundyense abundance and shellfish toxicity
in the Gulf of Maine, Deep-Sea Research II 52:28432855, 2005.
Pollard RT, et al.: Southern Ocean deep-water carbon export enhanced by
natural iron fertilization, Nature 457:577581, 2009.
Sievers AM: Comparative Toxicity of Gonyaulax monilata and Gymno-
dinium breve to annelids, crustaceans, molluscs and a fish, J Protozool
16(3):401404, 1969.
Zhang J: Atmospheric wet deposition of nutrient elements: correlation
with harmful biological blooms in Northwest Pacific coastal zones,
Ambio 23(8):464468, 1994.
Conclusion
Cells divide and that leads to population growth in unicellular organ
isms. Cell division and population growth illustrate how all cells come
from preexisting cells. Unicellular organisms can have wide-ranging and
important effects in ecological systems. Entire ecological systems can
be affected by just one species of unicellular organism. A population of
nitrogen fixing bacteria can provide the nitrogen essential for growth of
plants. Red tides, or HABs, occur in ecological systems because of favor
able ecological conditions, leading to conditions unfavorable for other
species. All of these effects are properties that emerge in ecological systems
from lower levels of biological organization. Emergent properties is a fun
damental concept of biology, one that will be explored in several other
books in this series.
Glossary
algal bloom. The rapid growth of a large population of algae.
assimilation. Assimilation is the process of absorbing nutrients and incorporating
them into the body.
carrying capacity. Carrying capacity is the maximum, equilibrium number of
organisms of a particular species that can be supported indefinitely in a given
environment.
cells. The smallest structural and functional unit of an organism.
death phase. The phase of population growth during which the population
declines.
decomposition. Decomposition is the decay into constituent parts by physical,
chemical, or biological processes.
denitrification. Denitrification is a microbially facilitated process of nitrate
reduction that produces molecular nitrogen.
detritivores. Animals that feed on dead plant or animal matter.
doubling time. Doubling time is the time it takes for a population to double in
number.
dynamics. In ecology, dynamics refers to changes over time and space, in popula
tions and ecological systems.
ecological systems. An ecological community together with the abiotic environ
ment, usually considered to function as a unit.
exponential growth. A type of population growth in which the amount being
added is proportional to the amount already present.
exponential phase. The phase of population growth in which exponential growth
occurs.
global climate change. The recent and ongoing rise in average global temperatures.
growth rate. Growth rate is the change in number of individuals per unit time.
harmful algal bloom (HAB). The rapid growth of a large population of algae
that produce and excrete chemicals that are harmful or toxic to other organisms.
iron hypothesis. The hypothesis that iron is the limiting nutrient to algal growth
in the open oceans.
lag phase. The phase of population growth in which the population is adjusting
to its environment, prior to the exponential phase.
logistic growth. A type of population growth in which the growth rate decreases
as the population nears carrying capacity.
microbes. Microscopic single-cell organisms, such as bacteria.
molecular. The level of the biological hierarchy that relates to, or consists of,
molecules.
46 GLOSSARY
nitrification. Nitrification is the conversion of ammonium to nitrite and nitrite

to nitrate.
nitrogen cycle. The nitrogen cycle describes the circulation and chemical reactions
of nitrogen in ecological systems.
nitrogen fixation. Nitrogen fixation is the conversion of atmospheric nitrogen
(N2) to ammonia (NH3)
nutrient cycles. Nutrient cycles are all the processes by which nutrients change
chemical form and are transferred from one part of an ecological system to
another.
ocean fertilization. Type of climate engineering where nutrients are introduced
to the upper ocean to remove carbon dioxide from the atmosphere.
organism. An individual animal, plant, or single-celled life form.
paralytic shellfish poisoning (PSP). A syndrome in which shellfish that have
themselves ingested neurotoxins in their food are then consumed by humans, and
lead to paralysis and other neurological symptoms.
phytoplankton. Plankton, microscopic organisms drifting or floating in water,
capable of photosynthesizing.
populations. A population is a group of individuals of the same species living in
the same place at the same time
protists. Protists are members of a group of eukaryotic, mostly unicellular organ
isms, including algae and protozoans.
red tide. A red tide is an algal bloom caused by dinoflagellates that color coastal
waters reddish.
spectrophotometry. uses the absorption of light to measure the concentration
and identity of chemical compounds.
stationary phase. The phase of population growth in which the population is at
its carrying capacity and growth rate is at or near zero.
wet deposition. Wet deposition is the process by which aerosol particles are
removed from the atmosphere by water droplets.
zooplankton. Plankton, microscopic organisms drifting or floating in water, that
are heterotrophic and consumers of other living organisms.
Index
Adenine triphosphate (ATP) Detritivores, 7
synthesis, 22 Dinoflagellates, 7, 8, 9, 27, 31, 3438
Agricultural practices, on soil Doubling time, 1, 4
ecosystems, 2326 Dynamics, xiii
A. klebsii, 7, 8
Alexandrium, 31, 37, 38 E. coli, 5
Alexandrium fundyense, xiii Ecological systems, xiii, 2225
Alexandrium minutum (A. minutum), Environmental pollution, 24, 31
3133, 37 Erosion, 25
Alexandrium monilatum Eukaryotic cells, 1, 7, 9
(A.monilatum), 3537 Exponential growth, 4
Algal bloom, 27 Exponential phase, 6
toxic, 2931, 35, 38
Amoeba, 7 Faba bean (Vicia faba), 11
Amphidinium carterae nitrogen content of, 12, 14
(A.carterae),7,8 Fertilizers, 2325
Assimilation, 20, 21
Global climate change, 25, 39, 40
Bacillus cereus, 1, 3, 4 Green revolution, 23, 25
Bacterium aerogenes, 1, 3, 4 Growth rate, 3, 4
Barley (Hordeum vulgare), 11 Gymnodinium breve (G. breve), 3537
nitrogen content of, 1213 Gyrodinium aureolum (G. aureolum),
Beans (Phaseolus vulgaris), 15 7, 8
Carbon sink, 3941 Harmful algal bloom (HAB).

Carrying capacity, 6, 35 SeeToxic algal blooms
Cell division, 13 Human population, 2325
Cells, xiii
Chemical pest control, 24 Industrialization, 31
Chickpea (Cicer arietinum) Inorganic fertilizers, 23
growth in actual field conditions,17 Intergovernmental Panel on Climate
nitrogen content of, 16 Change (IPCC), 39
Rhizobium affecting, 1617, 18 Iron hypothesis, 39, 40
Clover, 14, 15
Coastal waters, wet deposition of, 28 Karenia brevis, xiii
Death phase, 6 Lactobacillus plantarum

Decomposition, 20, 21 (L.plantarum), 5, 6
Denitrification, 2223 Lag phase, 6
Desertification, 25 Legume chickpea. See Cicer arietinum
48 INDEX
Legumes, 11, 1416, 24 Prokaryotic cells, 1

root nodules on, 15 Protists, 7
Logistic growth, 6
Red clover (Trifolium pratense), 15
Microbes, xiii Red tide, xiii, 2741
Molecular, xiii Response of chickpeas, 18
Rhizobium, 1520
Nitrification, 22 River water, concentrations in, 28
Nitrite accumulation, in bacterial
cultures, 2122 Saccharomyces ellipsoideus
Nitrobacter, 22 (S.ellipsoideus), 1, 3, 4
Nitrogen cycle, 1920 Salinity, salinization, 25, 33
Nitrogen fixation, 1214, 1619 Scrippsiella trochoidea, 7, 8
Nitrosococcus, 22 Soil ecosystems
Nitrosomonas, 22 agricultural practices on, positive/
Nonbiological nitrogen fixation, 13 negative consequences of,
Nutrient cycles, 19 2326
soil microbes in, 1126 Soil microbes, in nutrient cycling,
1126
Ocean fertilization, 40 ethical, legal, social implications
Ocean water, nutrients in, 28 of,2326
Organism, xiii Sorghum, 14
Spectrophotometry, 5
Paralytic shellfish poisoning (PSP), Stationary phase, 5, 67
xiii, 37, 38 Synthetic fertilizers, 23
Paramecium, 7
Pea (Pisum sativum), 11 Tilling, 25
nitrogen content of, 12, 14 Toxic algal blooms, 2931, 35, 38
Pesticides, 2325
Photosynthetically active radiation Unicellular organisms, 19, 27
(PAR), 34 United Nations Convention
Phytoplankton, 2741 on Biological Diversity
ethical, legal, social implications of, (UNCBD), 40
3941
Plankton, 27 Wet deposition, 28
Plasmodium, 7
Populations, xiii Zooplankton, 39
OTHER TITLES IN OUR BIOLOGY
COLLECTION
Behavior and Information Exchangeby Christopher J. Paradise and A. Malcolm Campbell

Cells in Tissuesby Christopher J. Paradise and A. Malcolm Campbell
Evolution of Interactions in Communitiesby Christopher J. Paradise and
A.Malcolm Campbell
Evolutionary Historyby Christopher J. Paradise and A. Malcolm Campbell
Effects of Genetic and Pathogenic Diseases on Cellsby Christopher J.Paradise and
A.Malcolm Campbell
Information in the Environmentby Christopher J. Paradise and A. Malcolm Campbell
Mechanisms of Evolutionby Christopher J. Paradise and A. Malcolm Campbell
Properties in and of Populationsby Christopher J. Paradise and A. Malcolm Campbell
Variation and Population Geneticsby Christopher J. Paradise and A. Malcolm Campbell
Ecological Homeostasisby Christopher J. Paradise and A. Malcolm Campbell
Ecological Interactionsby Christopher J. Paradise and A. Malcolm Campbell
Emergent Properties of Individual Organismsby Christopher J. Paradise and
A. Malcolm Campbell
Organismal Homeostasisby Christopher J. Paradise and A. Malcolm Campbell
Population Homeostasisby Christopher J. Paradise and A. Malcolm Campbell
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APPLIED BIOLOGY COLLECTION
Population growth, dynamics, and blooms of bacterial, unicel-
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Microbes are used to illustrate both exponential and logistic
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ics in other aspects of ecological systems, including nutrient
Ecological
Bundlethe more
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harmful algal blooms. Populations of harmful algal can quickly
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Biology Christopher J. Paradiseis professor of biology and environ-
Mathematics mental studies at Davidson College. He teaches introductory
Chemistry biology, ecology, entomology, and topical seminars on ecotoxi-
cology and renewable natural resources. He also occasionally
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EBOOKS Ecological Dynamics

FOR THE Christopher J. Paradise A. Malcolm Campbell

concurrent usage NC. He received national and international education awards:

Christopher J. Paradise, PhD

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First published in 2016 by

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Both prokaryotic and eukaryotic cells divide, although the methods

I first generation cell

second II I II second generation cell

fourth generation cells time for fourth division

Figure 1 Schematic of cell division for bacteria and yeast observed on

The first generation of cells in the population depicted in Figure 2A con

percentage of cells dividing

Figure 2 The proportion of cells dividing within a particular period of

20 minutes, x = 8 260/20 t = 8 23t. The multiple of t in the exponent

which is obtained from the model presented above (32.74 minutes

population, often both considered as constants for populations, were

phase occurs when a bacterial population runs out of an essential nutri

favorable to growth. As with the various bacteria species, some species

Monod J: The growth of bacterial cultures, Ann Rev Microbiol 3:371394,

Soil Microbes are Involved

Find a flower bed or vegetable garden and pick up a handful of soil.

phosphorus in quantities that would prevent growth of plants from being

Figure 3 Nitrogen content of aboveground portions of crops.

Table 1 Source of nitrogen for three crops. All values are

Source: From Seneratne and Hardason, 1988, multiple tables.

conversion of atmospheric nitrogen to ammonia is an energy intensive

roots vascular tissue

Figure 4 Root nodules on legumes. Shading in nodule cells show areas

To begin addressing this question, scientists examined the anatomy of

Figure 5 Nitrogen content of chickpea shoots grown hydroponically

Prior to planting, the outer surface of seeds were sterilized to kill

nodule dry mass per plant aboveground dry mass

Figure 6 Response of chickpeas to two fertilizer conditions or

The experiments by Beck showed that in the presence of rhizobia

Figure 7 The nitrogen cycle showing compartments that contain

to Rhizobium bacteria that convert it to ammonia and then incorporate it

cummulative nitrite (mg nitrite/day/100 ml)

Figure 8 Accumulation of nitrite in bacterial cultures provided with

If assimilation by plants requires nitrate, and nitrogen fixation and

The bacteria in these cultures appear to be converting ammonium to

where nitrate is used in place of oxygen as an electron acceptor in the

Ethical, Legal, Social Implications:

The downsides to use of industrialized produced nitrogen fertilizers

Certain Phytoplankton can

6 nutrient inputs to the Yellow Sea

Figure 9 Nutrient concentrations of water sources (A) and nutrient

Finally, the researchers at the stations recorded the dates, locations,

events (blooms) or deposition (nutrients) 35

= toxic bloom events (%)

25 = silicon dioxide (%)

Figure 10 Percentages of total toxic algal bloom events and total

Beginning in the late 1960s and continuing to today, Chinas

Figure 11 Maximum bloom of A. minutum over 3 years plotted

Maguer and his colleagues measured nutrient concentrations in the water

number of cells (3 106 L1) 30

Figure 12 Changes in cell densities of A. minutum during the algal

By studying a recurring bloom in one estuary off the coast of France,

the growing algal populations essentially stripped the ammonium from