Effects of Resource Distribution on Animal–Plant Interactions

502 Pages·1992·7.315 MB·English

by  Mark D. Hunter, Takayuki Ohgushi and Peter W. Price (Eds.)

Effects of Resource
Distribution on
Animal-Plant Interactions
Edited by
Mark D. Hunter
Department of Entomology
Pennsylvania State University
University Park, Pennsylvania
Takayuki Ohgushi
Shiga Prefectural
Junior College
Shiga, Japan
Peter W. Price
Department of Biological Science
Northern Arizona University
Flagstaff, Arizona
Academic Press, Inc.
Harcourt Brace Jovanovich, Publishers
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Copyright © 1992 by ACADEMIC PRESS, INC.
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Library of Congress Cataloging-in-Publication Data
Effects of resource distribution on animal-plant interactions /
[edited by] Mark D. Hunter, Takayuki Ohgushi, Peter W. Price,
p. cm.
Includes bibliographical references and index.
ISBN 0-12-361955-6
1. Animal-plant relationships. 2. Variation (Biology)
I. Hunter, Mark D. II. Ohgushi, Takayuki. III. Price, Peter W
QH549.5.E34 1992
574.5'24-dc20 91-24301
CIP
PRINTED IN THE UNITED STATES OF AMERICA
91 92 93 94 9 8 7 6 5 4 3 2 1
Preface
One major component of the complexity of natural biological systems is heter­
ogeneity. Even the most superficially homogeneous communities of animals
and plants exhibit considerable spatial and temporal variability when they are
examined closely. Although heterogeneity has been recognized in biological
systems for hundreds of years, incorporating much of this variability into our
understanding of the natural world is in its infancy. Until relatively recently,
for example, fields such as population and community ecology have essentially
ignored variation in time and space in their conceptual and theoretical models.
The purpose of this volume is to explore the importance of natural variabil­
ity in one field of biology—animal-plant interactions. Specifically, we argue
that our understanding of population, community, and evolutionary level
interactions between plants and the animals that depend on them are better
understood when heterogeneity is taken into account. The causes and conse­
quences of variability among plants as resources for animals (Chapters 4, 5, 6,
7, 9, 10, 14) and variability among animals as both resources for (Chapters 4,
11, 12, 13) and exploiters of plants (Chapters 2, 3, 4, 8) link all the contribu­
tions in this volume together. We suggest that many of the complex interac­
tions we perceive in natural animal-plant systems arise from the superim­
posing of herbivore variation upon plant variation.
Indeed, variability among the individual herbivores within a species is a
recurrent theme in this volume, and we explore the consequences of that
variability for plant pollination and reproductive success (Chapters 5 and 13),
animal population dynamics (Chapters 2 and 8), and animal social systems
(Chapter 3). The authors of these chapters express the view that individual
variation among herbivores within a species has important ramifications at
population, community, and evolutionary levels, and we predict that major
advances in animal—plant biology will result from the synthesis of studies at
these different levels of organization.
We think this volume should also stimulate more focused debate on the
relative strengths of bottom-up versus top-down effects in terrestrial food
webs. To what extent is pattern in plant-feeding species and communities
generated by plants and vegetation compared to carnivore effects? This theme
runs through the volume. Some chapters take a balanced approach by illustrat­
ing the tight interactive linkages between plant resources, herbivores, and
carnivores (Chapters 1, 7, 9, 10). Other chapters either debate the validity of
ix
X Preface
strong bottom-up effects that generate pattern (Chapters 4, 6) or discuss the
important role of resource display and variation in the evolution of life histo­
ries of animals exploiting plants (Chapter 12). Coupling such variation pro­
vided by plants to the necessarily opportunistic exploitation by pollinators
provides a constantly shifting set of relationships in bee communities (Chapter
11). In spite of the different approaches taken in these chapters, the logic of a
building-block approach, with plants as the autotrophic foundation, generates
a frame of reference that provides considerable comparative power across
diverse systems.
Another theme in this volume is inevitably the necessity of integrating the
abiotic environment into the understanding of plant and animal interactions.
This is most explicitly addressed in Chapter 14, but many of the chapters
invoke the importance of physical factors, not only in defining plant distribu­
tion and abundance, but as major mediating components in linkages among
trophic levels.
Although we have organized the chapters in this volume to reflect a natural
hierarchy of organization, from the individual to the community and evolu­
tionary level, there is considerable overlap between sections. We interpret this
as an encouraging sign of an emerging synthesis of ideas. Section I considers
genetic and phenotypic variability among animals and plants; Section II ex­
plores their reproduction and population dynamics; Section III investigates
patterns in animal-plant communities; and Section IV describes interactions
between animals and plants developed over evolutionary time.
We use the term "herbivore" in its broadest sense, to include frugivores, seed
predators, pollen and nectar feeders, as well as animals that consume leaves
and other vegetative parts. We have tried, where possible, to consider the
consequences of heterogeneity for animal—plant interactions in a variety of
animal taxa, including birds, bats, rodents, fish, and insects and to draw
generalizations where they emerge.
After a short introduction, the remaining chapters in this volume contain
brief literature reviews, descriptions of the author(s) current research interests,
and novel hypotheses or research directions. This "where we've been, where
we are, and where we ought to go" approach is designed to appeal to the widest
possible audience. We anticipate a readership of informed undergraduates in
the biological sciences who wish to survey a particular field, and graduate
students who wish to incorporate natural heterogeneity into the design of their
research projects, as well as professional animal—plant ecologists who will test
some of the particular hypotheses presented here. To this end, we have made
the language in this book as "jargon-free" as possible and accessible to biologists
with a wide range of interests and experience. Since explicit consideration of
heterogeneity in natural systems is a young and developing field, we hope that
readers will contact the authors directly with questions, comments, and ideas.
The original idea for this book grew out of the Fifth International Congress
of Ecology 1990, Yokohama, Japan, and although we invited several other
Preface XI
thors to contribute, we would like to thank the organizing committee for
bringing the core group together. Special thanks is due to Professor Shoichi
Kawano, who suggested the topic and who extended his warmest hospitality.
All chapters in this volume have been peer reviewed by colleagues outside
this project. We would like to extend our gratitude to the following for their
help, guidance, and criticism: Heidi Appel, Alan Berryman, Cathy Bach,
James Cresswell, Hugh Dingle, Niles Eldredge, Stan Faeth, Peter Feinsinger,
Ted Floyd, Doug Futuyma, Fred Gould, Brad Hawkins, David Inouye, Masao
Ito, Lorrie Klosterman, Jill Landsberg, William Lidicker, Tom Martin, Judy
Myers, Mary Power, Mark Rausher, Shoichi Sakagami, Ellen Simms, John
Thompson, Peter Turchin, Nick Waser, and Allan Watt.
Natural Variability in Plants
and Animals
Mark D. Hunter Peter W. Price
Department of Entomology Department of Biological Science
Pennsylvania State University Northern Arizona University
University Park, Pennsylvania Flagstaff, Arizona
I. Introduction
If the world were one continuous carpet of vegetation, equal in all ways as a
resource for animals, there would be no need for this book. In recent years,
however, more texts have begun to stress the variability of plants as a food
source and as shelter for the animals that they support (Rosenthal and
Janzen, 1979; Denno and McClure, 1983; Strong, Lawton and Southwood,
1984). From these and other sources has come the realization that we must
consider the distribution of quality as well as quantity of plants and plant
parts if we are to develop our understanding of plant-herbivore interac­
tions. Herbivores, too, exhibit significant genetic and phenotypic variability,
both within and between species. Variable herbivores, therefore, are likely
to exert ecological and evolutionary pressures on plants.
Variability is hierarchical. Most ecologists would agree that variation
among different species of plants has a considerable influence on the distri­
bution and abundance of herbivores. We know much less about the effects
of heterogeneity among plant populations and individuals on the animals
that depend upon them. Our level of understanding is poorer still when it
comes to the converse; we know surprisingly little about the effects of
variation among herbivore populations and individuals on plant ecology
and evolution. However, we might expect that many of the complex pat­
terns we see in animal-plant systems arise from interactions between hetero­
geneous plants and heterogeneous herbivores.
Copyright © 1992 by Academic Press, Inc.
Effects of Resource Distribution on Animal-Plant Interactions "J All rights of reproduction in any form reserved.
2 Mark D. Hunter and Peter W. Price
Figure 1 is a simplified representation of the major factors that generate
variability in plants and herbivores. We feel that this model is applicable at
the individual, population, or species level. In the model, plant heterogene­
ity arises from variability among herbivores, climate, soils, plant pathogens,
decomposers, and symbionts. We have ignored genetic mutation because we
assume, for the sake of simplicity, that the prevalence of particular plant
genotypes reflects natural selection acting through the other factors men­
tioned above.
Likewise, herbivore heterogeneity arises from variability among plants,
natural enemies (including pathogens), climate, and symbionts. A more
complex (and realistic) model might represent the relative strengths of these
forces by the thickness of the arrows on Figure 1. However, we simply do not
have sufficient information to do this for any natural system of which we are
aware. That mycorrhizae (Siqueira etaL, 1989) and plant pathogens (Power,
1991) can influence plant heterogeneity is almost certain, but the relative
strength of their effects compared to, for example, climate is unkown.
One purpose of this book is to investigate the "thickness of the lines"
between herbivores and plants on Figure 1. We want to explore the conse­
quences of variability among plants for herbivores and the consequences of
variability among herbivores for plants. Currently we know more about the
former than the latter, and the contents of this book necessarily reflect that
unfortunate bias. Even excluding variability among herbivores, there is
remarkably little known about the effects of defoliation, especially below
ground (Reichman and Smith, 1991), on plant population dynamics and
community structure (Crawley, 1989). We would like to make a plea for
considerable expansion in this area of research.
We see a strong parallel between our current inability to determine the
relative thickness of the lines on Figure 1, and the debate between the
strengths of "bottom-up" and "top-down" forces in natural populations and
communities. There remains considerable disagreement in terrestrial sys­
tems, for example, about the relative roles of resource distribution and
natural enemies in determining herbivore population dynamics and com­
munity structure (Hairston et ai, 1960; Lawton and Strong, 1981; Faeth,
1987; Price, 1990). Part of this disagreement may arise from a lack of
appreciation for the degree of variability at lower trophic levels, and how it
can interact with species at higher trophic levels (Price et ai, 1980; Kareiva
and Sahakian, 1990). A simple genetic mutation in pea plants, for example,
can determine the efficacy of a natural enemy on its herbivorous prey
(Kareiva and Sahakian, 1990).
We would emphasize, therefore, that variability at lower trophic levels can
have cascading effects up the trophic system. This is not meant to deny the
power of "top-down" processes in many communities and several chapters
in this volume consider such effects. Rather, we wish to reestablish the
fundamental role of energy flow up through the system as the template
/. Natural Variability in Plants and Animals 3
ABIOTIC SYMBIONTS
VARIABILITY
'NATURAL ENEMY VARIABILITY
A
ABIOTIC SYMBIONTS
VARIABILITY
Y
/
> HERBIVORE VARIABILITY
A
ABIOTIC PLANT PATHOGENS SYMBIONTS
/
VARIABILITY
4
1/ 7
PLANT VARIABILITY
A 1
DECOMPOSERS
Figure 1 Major ecological forces that generate variability among plants and animals in
natural systems. Both abiotic and biotic forces can "cascade" up and down the trophic web so
that the action of climate on a natural enemy complex, for example, can influence the distribu­
tion and abundance of plants and even decomposers.
upon which all species interactions, "top-down" or "bottom-up" necessarily
take place. A balanced view on the relative roles of "top-down" and "bottom-
up" forces has emerged in aquatic systems (Carpenter et al, 1985, 1987;
McQueen et al, 1986, 1989; Schindler, 1978), and we hope to stimulate a
similar synthesis in terrestrial systems by emphasizing how variability in
plants can influence interactions at higher trophic levels.
Having listed major factors that generate variability in plants and animals
(Fig. 1), we will end this Introduction by reviewing briefly some of the
known causes and consequences of variability among primary producers.
We will leave it to other authors in this volume to describe the causes and
consequences of variability among herbivores, and to consider the benefits
of integrating a knowledge of variability at both trophic levels for our
understanding of animal-plant interactions.
A. Sources and Patterns of Plant Variability
1. Presence or Absence of the Host Plant
Of critical importance to specialist herbivores, and of varying importance to
oligophagous and polyphagous herbivores, is the presence or absence of a
particular plant species. Even at this fundamental level, there is a continuum
of spatial scales to be considered—the factors that make the pedunculate
4 Mark D. Hunter and Peter W. Price
oak Quercus robur L. widely distributed in Europe and absent from North
America are not the same factors that, for example, determine its presence
or absence in a particular woodland in Scotland. There are probably a
hierarchy of factors that reduce a plant's distribution from its "potential" to
its "realized" distribution ranging from climate, topography, and elevation,
to dispersal, soil variability, microclimate, competition, and herbivory. Bar­
tholomew (1958) considered that the biotic or abiotic factor to which an
organism has least adaptability or over which it has least control will ulti­
mately determine its distribution. This slight modification of Liebig's Law of
the Minimum (Liebig, 1840; Odum, 1959) is a rather static picture and, in
reality, the forces that determine plant distribution are dynamic in ecologi­
cal and evolutionary time. The generation of light gaps in tropical forests by
the death of canopy trees, for example, plays a critical role in the regenera­
tion of some tree species (Denslow et al, 1990 but see Welden et al, 1991).
Plant succession, of course, describes a turnover of species with time and
adaptation, too, can lead to the occurrence of plants in novel or hostile
environments (Antonovics et al, 1971). The more dynamic view of vege­
tation, and therefore resources for herbivores, was certainly fostered by
Loucks' (1970) view of periodic perturbation as an essential generator and
preserver of heterogeneity, and acted as a precursor to the now active study
of patch dynamics (e.g. Pickett and White, 1985).
Given the considerable variability in patterns of plant distribution, the
consequences of these patterns for herbivores are understandably complex.
The relationships among climate, plant distribution, and plant-herbivore
interactions are poorly documented, although there is growing evidence
that the evolution of host plant choice may be influenced by biogeographic
patterns and plant hybrid zones (Whitham, 1989; Boecklen and Spellen-
berg, 1990; Scriber and Lederhouse (Chapter 14)). Although the use of
island biogeography theory to explain the numbers of herbivores associated
with individual plants, plant populations, and plant species has received
some criticism (Kuris et al, 1980), there is good evidence that plant distribu­
tion and abundance can influence the biomass and species richness of
herbivores associated with primary producers (Southwood, 1960, 1961;
Root, 1973; Strong, 1979). Other studies, however, have suggested that a
diversity of host plant species may actually be important to particular herbi­
vores. For example, some monkeys are known to include plant species of
apparent low quality in their diet, perhaps in order to accumulate specific
nutrients (Oates et al, 1980).
The influence of plant succession on resource use by herbivores has
received more attention, and effects on plant palatability, herbivore special­
ization, and arthropod community structure have been described (Reader
and Southwood, 1981; Futuyma, 1976; Haeringand Fox, 1987). Given that
natural perturbations can generate patches of vegetation in varying stages
of succession, we should not be surprised to find that disturbances such as
1. Natural Variability in Plants and Animals 5
flooding (Power et ai, 1985) and drought (Young and Smith, 1987) can have
significant indirect impacts on animal populations and communities. When
perturbations influence patterns of plant succession, the consequences for
animals need not be restricted to herbivores. Pianka (1989), for example,
has suggested that the maintenance of species diversity in lizard commu­
nities in Australia is dependent upon regeneration of spinifex grassland,
which is dominated by fire.
Within a habitat, the spatial distribution of plants is often critical to
plant-herbivore interactions. For example, in temperate forests the proba­
bility of a plant's nearest neighbor being a conspecific is many times higher
than it would be in the majority of tropical forests. As a consequence,
herbivore dispersal strategies, their population dynamics, host plant choice,
and plant defensive strategies can vary dramatically with the diversity of the
plant community (Gilbert, 1975, 1979; Crawley, 1983). The density of
particular plant species within a habitat, either because they are unusually
beneficial or unusually deleterious, can be of enormous importance in
determining patterns of herbivore population change. The presence of oak
species (particularly chestnut oak) is strongly associated with outbreaks of
the gypsy moth in the north eastern United States (Houston and Valentine,
1977; Doane and McManus, 1981).
2. Temporal Variability
Plants as resources for animals can vary greatly during a year. Annual plants
may be absent for extended periods, and specialist herbivores have evolved
life cycles accordingly. The availability of plant parts is often highly sea­
sonal: pollen, fruits, seeds, buds, and the leaves of deciduous trees are
examples. The migration of ungulates (Sinclair, 1985), the narrow larval
feeding period of some phytophagous insects (Feeny, 1970; West, 1985),
and the spawning of marine invertebrates (Starr et ai, 1990) can all be
viewed as adaptations that exploit a temporally variable plant resource.
Seasonal variation in the quantity or quality of plants and plant parts can
have direct effects on the growth, reproduction, and movement of herbi­
vores (Feeny, 1970; Rockwood, 1974; Haukioja and Niemela, 1979;
Ramachandran, 1987) or indirect effects by their interaction with climate or
natural enemies (Price et al, 1980; Schultz, 1983; Hunter, 1987). The
quality of plants as a resource for animals can vary over a much shorter time
period too. Diurnal changes in flower availability are common, and contin­
ual changes in the nectar supply of some species are known to influence the
behavior and foraging strategy of pollinator species (Gill and Wolf, 1975).
The consequences of seasonal variability in the quantity and quality of
plants and plant parts has been investigated most thoroughly for phytopha­
gous insects (e.g. Strong et al, 1984). Many studies suggest that, in general,
foliage quality declines with age due to decreasing water content and in­
creasing toughness (Feeny, 1970; Wint, 1983). The effects of leaf age on leaf