The Inadequate Environment: Nitrogen and the Abundance of Animals

436 Pages·1993·8.21 MB·English

by  Thomas C. R. White (auth.)

T. C. R. White
The Inadequate
Environment
Nitrogen and the Abundance of Animals
With 41 Figures
Springer-Verlag
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Thomas C. R. White
Dept. of Crop Protection
Waite Agricultural Research Institute
Glen Osmond, South Australia
5064 Australia
ISBN-13:978-3-642-78301-2 e-ISBN-13:978-3-642-78299-2
DOl: 10.1007/978-3-642-78299-2
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© Springer-Verlag Berlin Heidelberg 1993
Softcover reprint of the hardcover 1st edition 1993
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To the memory
of my two mentors
H. G. (Andy) Andrewartha and
G. B (Joe) Rawlings
Acknowledgements
My story is, inevitably, built upon the ideas and research of others -
from Darwin to Dawkins - as reflected in my references. However,
there are some whose influence has been general rather than specific,
others of whose direct influence I am no longer conscious; still others
whose relevant work I have never encountered. To all these I apologize
for failing to acknowledge them.
The basic outline of my thesis finally crystallized while I was
teaching ecology at the University of the South Pacific in Fiji, and it
was Hermann Remmert's enthusiastic badgering which started me
putting it into book form. But I was only able to properly address the
task after retirement, and with the support of an honorary research
fellowship at the Waite Agricultural Research Institute.
For many years I worked where ready access to the literature was
limited. lSI's Current Contents, and the hundreds of reprints sent to
me by colleagues throughout the world enabled me to keep up.
Too many colleagues to list lent photographs to illustrate the book
- mostly colour slides. Jennie Groom did a grand job producing
black and white prints from the latter. Many of these same colleagues,
and several others, also helped with comments on appropriate sec
tions. Tom Browning read much of an early draft, alerting me to
grammatical slips and lapses into teleology. But I continue to
deliberately split an occasional infinitive, and resort to teleological
analogy if I think this makes for clearer exposition!
However, it has been Piet den Boer, with his detailed and wise
criticisms via our lengthy discussions by post, who has done more
than anybody else to improve both what I have to say, and the way
in which I say it. I am especially grateful to him.
To all, my very sincere thanks, coupled with the usual exoneration
from any responsibility for what I have said. And in this age of word
processors I can blame nobody but myself for typing and spelling er
rors!
Last, my very special thanks to my wife, Janice, for grammatical
advice, painstaking assistance with final much valuable proof-read
ing, and, above all, for continuing to believe in the worth of the pro
ject, and for keeping me at it on the numerous occasions when I lost
my confidence.
Preface
This is not a text book. Nor is it an objective review. It is a personal
- and thus biased - view of some facets of ecology; a view I
vigorously advocate. More specifically, it is an attempt to report pat
terns that I perceive threaded through the fabric of the living world,
the common cause of those patterns, and some of the implications
for our understanding of ecology that flow from this perception. As
a result I come to conclusions that sometimes differ from much that
is generally accepted, and with which many will not agree. But I have
not felt obliged to put the case for alternative hypotheses or inter
pretations. I leave those who support them to expound their own
viewpoints.
In advocating my viewpoint I have taken examples from studies
that cover a wide geographic and taxonomic range. However, I have
not attempted to be comprehensive. Such would have been a futile
task, even had I the energy, or time left, to try to do so. Every story
I follow up uncovers several new ones. Yet there remains a majority
of the literature that I have never seen - and never will.
Apart from this, however, there is simply not room for all the ex
amples that I have found. If I reported these, the book would be dou
ble its size, so I have had to knowingly put much good evidence on
one side. For example, I have left out major groups like the mites and
the nematodes, and the sawflies and leafbeetles among the insects.
Some, like the bacteria, get inadequate coverage; others, like the bark
beetles, get but passing mention. And within the groups from which
I have taken examples, there are many more cases that I could equally
have reported.
Furthermore, I have not tried to be even-handed in selecting which
out of so many examples to use. Rather, I have tried to select studies
which tell a reasonably complete story, or which make a particular
point unambiguously. For all these reasons what I have to say is in
complete and patchy, but I hope that what I have chosen illustrates
the generalities sufficiently, and that others will fill in the gaps.
In attempting to write clearly and simply I have eliminated
acronyms, all but common abbreviations, and as much jargon,
technical language, and quantitative detail as possible. I have balanc
ed the latter, however, with a very full bibliography wherein the reader
who so wishes can find these details.
x
Preface
One of the temptations in modern ecological research is to retreat
within the protective jungle of complexity. For some, the natural
world seems so diverse, and interactions within it so varied, that they
believe we cannot expect to find general patterns there. Unlike phys
ics, they say, there can be no hard laws of ecology that will encompass
the ever-growing diversity of life; every case will be different. Many
delight in this diversity, and present evidence for it in detailed descrip
tions of the structure of, and interactions within, ecosystems, com
munities, food webs, and populations.
However, I believe that the task of ecologists is to do more than
describe - no matter how precisely and quantitatively. Like other
scientists we must search for rules that are more general than others,
and which explain the complexity and variability we observe. This
book is my attempt to contribute to that process.
My colleague Piet den Boer warns me, however, that we cannot
make science by piling up selected examples. I agree. But by presen
ting a broad cross-section of examples I can best demonstrate the ex
istence of general patterns in nature. A knowledge of these patterns
allows the derivation of new, testable hypotheses about their cause.
These, in turn, will lead to the making of more science.
This is especially so if they are primary patterns. Feeding on flush
tissues, coprophagy, or the early death of most young, for example,
are some of the primary ecological patterns that I perceive to be
reflecting the common scarcity of nitrogenous food. They are
analogous to primary evolutionary patterns, like the skeletal structure
of vertebrates, which reflect a common ancestry. Understanding them
may also help interpret secondary ecological patterns, like those
found in the interrelations within communities and food webs, or in
guilds of animals associated with vegetational succession.
Others will protest that there are many exceptions which I have not
presented. But, as Peter Price (1991a) recently pointed out, exceptions
cannot destroy the existence of a pattern - they cannot disprove it.
This can be done only when the preponderance of evidence shows
that another pattern - or no pattern - exists. Furthermore, many
exceptions, when more carefully investigated, prove not to be excep
tions at all. They are either reconcilable with the rule they seemed to
contradict, or they lie outside of it.
There are two basic concepts that underpin what I have to say: the
oneness of life; and the importance of the individual. And I do not
use either expression in any emotional or anthropomorphic sense;
quite the reverse.
The enormous diversity of form, function, and interaction of life
that we observe today is all part of one pullulating, mindless con
tinuum; the whole evolved from the same simple, early replicators,
and programmed and driven by their descendent genes to produce
even more genes in the future. [Dawkins (1986, 1989) says all this
Preface XI
much better than I). Natural selection operates upon the consequent
"oversupply" of individual phenotypes, eliminating all that cannot
cope. The death of so many is not "wasteful", nor cause for sentimen
tal concern. Nature has no "thought" for the "welfare" of future
generations. Natural selection, while determining the future, is yet a
process for the moment.
Because this is the way nature works, the individual phenotype
should be paramount in ecological studies. The environment of an
organism is everything that impinges upon it, including those of its
own kind (Andrewartha 1970). As Einstein is purported to have said,
"The environment is everything that is not me". All of nature com
prises individual phenotypes each struggling to survive in its own in
differently harsh environment. It is essential that we think about
ecological interactions from the point of view of that individual's
struggle.
All that said, this book is mostly about herbivores. Not because
they are more "important" than carnivores, but because it is not
widely recognized or accepted, as it is for carnivores, that herbivores
are limited by their food - even less that it is nitrogen, not energy,
which is in critically short supply for them.
This is the heart of my thesis. A lack of access to nitrogen in a
form that can be used for the production and growth of young is the
major restriction on the abundance of all animals. This shortage is
reflected in a host of common structural, physiological, and
behavioural adaptations, which all serve the same function of helping
alleviate this "universal nitrogen hunger" (Keeble 1910).
Many years ago my friend and colleague Alan Newsome, who has
worked all his life with mammals, told me that, for him, insects might
just as well be Men from Mars! Mindful that there are many
ecologists like him, I have arranged and subdivided the text so that
those who wish to find out what I have to say can do so without read
ing about very much other than "their" animals. But I would plead
with them not to stop there. I think they will find that animals which
they have never encountered, or have had little to do with since their
undergraduate days have, ecologically, much in common with the
animals that they work with every day. Then, if I have been half-way
successful in gathering and presenting the evidence, they will begin to
see the generality of my thesis.
Finally, I did not write this book solely for my fellow ecologists.
I hope that many others will find what I have to say both useful and
enjoyable to read. And students, too, both postgraduate and
undergraduate - those who are not yet set in their thinking like we
older ones. To them I say: read this, think about it, and then go and
look at the world from this point of view. The evidence is there.
Adelaide, November 1992 T. c. R. White
Contents
Part I: The Inadequate Environment
Introduction .......................................... 3
Chapter 1. The Environment of All Organisms
Is Inadequate ......................................... 5
1.1 Natural Selection Is a Negative Process ............... 6
1.2 Populations Press Against Limits of a Minimum
Resource... .. .... . . .. .... . .... .... .... ..... ...... . 8
1.3 What Essential Resource Is Most Likely to Be Limiting? 11
1.3.1 Nitrogen the Most Limiting Chemical ........... 11
1.3.2 Nitrogen Limiting Plants ...................... 12
1.3.3 Nitrogen Limiting Animals ..................... 13
1.3.4 Energy Not Limiting .......................... 14
1.4 Competition a Consequence Not a Cause ............. 14
1.4.1 Intra-specific Competition ..................... 14
1.4.2 Inter-specific Competition and "Competitive
Exclusion" ................................... 16
1.5 Self-regulation Does Not Exist ... . . . . . . . . . . . . . . . . . . . . 20
Chapter 2. Plants as Food for Herbivores ................ 22
2.1 Why Is the World Green? ........................... 22
2.2 How Might Plants Be an Inadequate Source of Food? .. 23
2.3 How and When Might Nutrients in Plants
Be Too Dilute? .................................... 23
2.4 When Is a Minimum Supply of Nitrogen
Critically Important? ............................... 24
2.5 How Might Herbivores Counter the Plants' Evolved
Strategies? ........................................ 24
2.6 How General Is Dilution of Nitrogen in Herbivore Food,
and What Adaptations Have Evolved to Counter it? ... 26
XIV Contents
Part II: Herbivores in an Inadequate Environment
Chapter 3. Insects ..................................... 31
3.1 Flush and Senesence Feeders ........................ 32
3.1.1 Two Australian Psyllids on Eucalyptus .......... 34
3.1.2 Two African Scale Insects on Californian Ice
Plants ...................................... 37
3.1.3 Two Aphids on Scots Pine .................... 38
3.1.4 The Green Spruce Aphid in Scotland. . . . . . . . . . . 39
3.1.5 Aphids on Sycamore, Apple, Wheat, and Alfalfa 41
3.1.6 Scale Insects on Euphorbia and Euonymus ...... 42
3.1.7 A Leafhopper with Alternate Generations
on Brambles and Oak ........................ 43
3.1.8 Two Species of Caterpillars Eating Oak Leaves .. 44
3.1.9 Two Species of Sawflies Mining in Birch Leaves. 45
3.1.10 A Chewer and a Sucker on Poplar Leaves. . . . . . . 46
3.2 Leaf-miners ....................................... 48
3.2.1 The Switch from Flush to Senescence Feeding ... 48
3.2.2 Leaf-miners Which Induce "Green Islands"
in Leaves ................................... 49
3.2.3 A New Zealand Weevil Mining in Fallen
Beech Leaves ................................ 49
3.2.4 The American Holly Leaf-miner ............... 50
3.3 Gall Makers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
3.3.1 Physiological Galls ........................... 53
3.3.2 Nutritional Benefits of Galling ................ 54
3.3.3 Adaptive Nature of Galls Debated Anew ........ 55
3.3.4 Double-dipping: Prolonged Growth plus Hastened
Senescence .................................. 57
3.3.5 Selection for High Nitrogen and Survival
of the Young ................................ 58
3.3.6 Selection of Growing Tissues for Proliferation
of Galls .................................... 61
3.4 Chewing Insects ................................... 62
3.4.1 Creaming-off as a Tactic to Increase Access
to Nitrogen: White Butterflies on Crucifers ..... 63
3.4.2 Early Instars Need More Nitrogen: Gypsy Moth
on Artificial Diet ............................ 65
3.4.3 Illustrations from the Life Cycles of Economically
Unimportant Butterflies ...................... 65
3.4.4 Further Examples from Forest Defoliators ....... 70
3.4.5 Pests of Crops also Reveal the Need for Nitrogen 75
3.4.6 Examples from Biological Control of Weeds .... 77
3.4.7 Locusts and Grasshoppers .................... 80
3.5 Sap-Sucking Insects ................................ 85