Parasitoid Population Biology

By Michael E. Hochberg and Anthony R. Ives

Extraordinary in the diversity of their lifestyles, insect parasitoids have become extremely important study organisms in the field of population biology, and they are the most frequently used agents in the biological control of insect pests. This book presents the ideas of seventeen international specialists, providing the reader not only with an overview but also with lively discussions of the most salient questions pertaining to the field today and prescriptions for avenues of future research.


After a general introduction, the book divides into three main sections: population dynamics, population diversity, and population applications. The first section covers gaps in our knowledge in parasitoid behavior, parasitoid persistence, and how space and landscape affect dynamics. The contributions on population diversity consider how evolution has molded parasitoid populations and communities. The final section calls for novel approaches toward resolving the enigma of success in biological control and questions why parasitoids have been largely neglected in conservation biology. Parasitoid Population Biology will likely be an important influence on research well into the twenty-first century and will provoke discussion amongst parasitoid biologists and population biologists.


In addition to the editors, the contributors are Carlos Bernstein, Jacques Brodeur, Jerome Casas, H.C.J. Godfray, Susan Harrison, Alan Hastings, Bradford A. Hawkins, George E. Heimpel, Marcel Holyoak, Nick Mills, Bernard D. Roitberg, Jens Roland, Michael R. Strand, Teja Tscharntke, and Minus van Baalen.

• Language: English
• Publisher: Princeton University Press
• Release date: May 11, 2021
• ISBN: 9780691230894

Book preview

PARASITOID POPULATION BIOLOGY

PARASITOID POPULATION BIOLOGY

Edited by

Michael E. Hochberg and Anthony R. Ives

PRINCETON UNIVERSITY PRESS PRINCETON AND OXFORD

Copyright © 2000 by Princeton University Press

Published by Princeton University Press, 41 William Street,

Princeton, New Jersey 08540

In the United Kingdom: Princeton University Press, 3 Market Place,

Woodstock, Oxfordshire 0X20 1SY

All Rights Reserved

Library of Congress Cataloging-in-Publication Data

Parasitoid population biology / edited by Michael E. Hochberg and Anthony R. Ives,

p. cm.

Includes bibliographical references (p. ).

ISBN 0-691-04981-5 (cloth : alk. paper) — ISBN 0-691-04982-3 (pbk. : alk. paper)

eISBN 978-0-69123-089-4 (ebook)

1. Parasitoids. 2. Insect populations. I. Hochberg, Michael E. II. Ives,

Anthony R., 1961–

QL496.12.P37 2000

595.717'857—dc21 00-020748

www.pup.princeton.edu

R0

To Julien, Kévin, Joëlle, and Mary Ann

Contents

Preface  xi

List of Contributors  xiii

One

Introduction  3

Michael E. Hochberg and Anthony R. Ives

PART ONE: POPULATION DYNAMICS  15

Two

Host Location and Selection in the Field  17

Jérôme Casas

Three

Effects of Parasitoid Clutch Size on Host-Parasitoid Population Dynamics  27

George E. Heimpel

Four

Host-Parasitoid Models: The Story of a Successful Failure  41

Carlos Bernstein

Five

A Field Guide to Studying Spatial Pattern Formation in Host-Parasitoid Systems  58

Susan Harrison

Six

Parasitoid Spread: Lessons for and from Invasion Biology  70

Alan Hastings

Seven

Landscape Ecology of Parasitism  83

Jens Roland

PART TWO: POPULATION DIVERSITY  101

Eight

The Evolution of Parasitoid Egg Load  103

Minus van Baalen

Nine

Host Resistance, Parasitoid Virulence, and Population Dynamics  121

H. C. J. Godfray

Ten

Developmental Traits and Life-History Evolution in Parasitoids  139

Michael R. Strand

Eleven

Host Specificity and Trophic Relationships of Hyperparasitoids  163

Jacques Brodeur

Twelve

Comparing Parasitoid-Dominated Food Webs with Other Food Webs: Problems and Future Promises  184

Marcel Holyoak

Thirteen

Species Coexistence in Parasitoid Communities: Does Competition Matter?  198

Bradford A. Hawkins

PART THREE: POPULATION APPLICATIONS  215

Fourteen

Biological Control: The Need for Realistic Models and Experimental Approaches to Parasitoid Introductions  217

Nick Mills

Fifteen

Parasitoid Populations in the Agricultural Landscape  235

Teja Tscharntke

Sixteen

Threats, Flies, and Protocol Gaps: Can Evolutionary Ecology Save Biological Control?  254

Bernard D. Roitberg

Seventeen

What, Conserve Parasitoids?  266

Michael E. Hochberg

Eighteen

Conclusions: Debating Parasitoid Population Biology over the Next Twenty Years  278

Anthony R. Ives and Michael E. Hochberg

References  305

Index  359

Preface

HOST-parasitoid systems are being employed at an ever-increasing rate as models of evolution, population and community dynamics, species diversity, and biological control. Thus, we hope that this volume is timely, both to give a constructively critical review of past work and to propose new and interesting venues for future research. We decided that an exciting way to achieve this was to ask each contributor to discuss a subject about which he or she has strong opinions, particularly if the subject is poorly represented in the current literature. We were looking for fresh perspectives on a growing field.

With our invitation to contribute to this book, we gave contributors the following rules: Each chapter could have only a single author; this ensures that the ideas expressed in the chapters are not open to veto by coauthors. Each chapter should begin by presenting a brief review of empirical and theoretical work. Based on this review, the author should identify what he or she feels is the most exciting element for future research. This could be a question that remains unanswered, one that has been answered unsatisfactorily, or one unanswered from another field and that could be better pursued using parasitoids as model systems. The author should discuss in detail why the question is interesting and important, and make some headway toward proposing solutions. This could include a literature review, a comparative analysis, an analysis or re-analysis of data, and/or the development of mathematical models. The chapter should close with a short, critical discussion of what we should hope to achieve over the next twenty years or so.

We leave it to you to judge, based on this sample of perspectives (chapters 2 through 17) and our own perspectives (chapters 1 and 18), the state of parasitoid population biology research today and where it is going tomorrow.

We express our sincere thanks to the people of Princeton University Press for their encouragement and efficient help in the production of this book.

Michael E. Hochberg

Anthony R. Ives

April 1999

List of Contributors

Carlos Bernstein. Biométrie et Biologie Evolutive, Université Claude Bernard-Lyon I, 43 Bd. du 11 Novembre 1918, 69622 Villeurbanne, France

Jacques Brodeur. Centre de Recherche en Horticulture, Département de Phytologie, Université Laval, Sainte-Foy, Québec, G1K 7P4, Canada

Jérôme Casas. Institut de Recherche sur la Biologie de l’Iinsecte, IRBI-CNRS ESA 6035, Université de Tours, 37200 Tours, France

H. C. J. Godfray. Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK

Susan Harrison. Department of Environmental Science and Policy, University of California, Davis, CA 95616, USA

Alan Hastings. Department of Environmental Science and Policy, University of California, Davis, CA 95616, USA

Bradford A. Hawkins. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA

George E. Heimpel. Department of Entomology, University of Minnesota, St. Paul, MN 55108, USA

Michael E. Hochberg. Institut des Sciences de l’Evolution, Université Montpellier 2, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France

Marcel Holyoak. Department of Entomology, University of California, Davis, CA 95616–8584, USA

Anthony R. Ives. Department of Zoology, University of Wisconsin, Madison, WI 53706, USA

Nick Mills. Department of Insect Biology, University of California, Berkeley, CA 94720–3112, USA

Bernard D. Roitberg. Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada

Jens Roland. Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada

Michael R. Strand. Department of Entomology, University of Wisconsin, Madison, WI 53706, USA

Teja Tscharntke. Agroecology, University of Göttingen, Waldweg 26, D-37073 Göttingen, Germany

Minus van Baalen. Institut d’Ecologie, Université Pierre et Marie Curie, 7 quai St. Bernard, 75252 Paris Cedex 05, France

PARASITOID POPULATION BIOLOGY

One

Introduction

MICHAEL E. HOCHBERG AND ANTHONY R. IVES

ACCURATELY communicating where we are and where do we go from here is difficult in any discipline. This is particularly true for parasitoid population biology, because it is a relatively new and still diffuse field. The term parasitoid was coined less than one hundred years ago, and only in the past two decades has the term been widely accepted by biologists. Furthermore, population biology as we know it today is essentially a product of the last three or four decades. With relatively little history, it is difficult to predict how the field will develop in the future.

It is not our intention to give an extensive historical recast of parasitoid population biology; there are numerous books that already do this, and interested readers are referred to Hassell (1978), Price (1980), Waage and Greathead (1986), LaSalle and Gauld (1993), Godfray (1994), Hawkins (1994), Hawkins and Sheehan (1994), Jervis and Kidd (1996), Quicke (1997), Barbosa (1998), and Hawkins and Cornell (1999). Rather, we believe that it is now time to dedicate a volume to asking how satisfactory our current understanding is and discussing the prospects for research into the twenty-first century.

This book is composed of three parts: population dynamics, population diversity, and population applications. These rubrics reflect three main endeavors involving parasitoids. Population dynamics concerns how abundance changes in space and time, and what factors may be responsible for these changes. Parasitoid-based models are the most often used for understanding the population dynamics of exploiter-victim systems. Population diversity is the number and range of biologies that one finds within populations, assemblages of parasitoid species, and entire ecological communities. Here, parasitoids have established themselves as the prima facie model for diversity amongst the metazoa. Finally, population applications are the means by which parasitoids have found their way into the human world, usually in a positive fashion (e.g., as biological control agents), but sometimes in a negative one (e.g., as biological control agents that inadvertently attack nontarget species). Although parasitoids are the most employed agents for the biological control of insect pests, many still regard their application as much of an art form as a science.

Population Dynamics

For many population biologists, mention of the Nicholson-Bailey model conjures thoughts of instability and irrelevance. This has often led to its rejection as a useful descriptor of population dynamics. Nevertheless, we would argue that the vast majority of theoretical developments on parasitoid population biology unavoidably have antecedents in the work of A. J. Nicholson and V. A. Bailey (Nicholson and Bailey 1935; Bailey et al. 1962)¹. Nicholson and Bailey demonstrated that the most basic property of host-parasitoid systems—persistence—is not an easy thing to explain, thus generating a legacy of attempts to explain persistent natural systems.

Although a range of models are often presented as Nicholson-Bailey equations, the form accepted by most population ecologists is

N and P are densities of host and parasitoid, respectively, which change from generation t to t + 1 if the system is not exactly at equilibrium. F is known as the finite or net rate of increase of the host population (i.e., host growth rate when the parasitoid is absent from the system), a is the area of search of the parasitoid, and c is the number of female adult parasitoids produced per parasitized host. Hassell (1978) and, more recently, Mills and Getz (1996) discuss the development of the model.

The Nicholson-Bailey model poses an interesting puzzle: This, the simplest dynamic model for a tightly coupled host-parasitoid interaction, predicts growing population oscillations until the parasitoid becomes extinct due to sheer low densities, and the host either becomes extinct due to the action of the parasitoid, or exhibits unchecked growth if the parasitoid should become extinct first. Since it is obviously the case that some parasitoid populations exist, there must be one or more essential elements that are missing from the Nicholson-Bailey model. Thus, the problem boils down to knowing the range of biological, ecological, and environmental complexities needed for interacting parasitoids and hosts to persist. The challenge to population biologists has been to identify and evaluate the various possibilities.

What the overwhelming majority of models indicate is there must be density dependence, but not just of any form. For example, density-dependent reductions in parasitoid attack rates leading to a type II functional response tends to make the Nicholson-Bailey model even less stable. In contrast, density dependence increases stability when the parasitoid population experiences contest competition (Taylor 1988b), when the parasitoid inflicts mortality on the host in a heterogeneous fashion (Chesson and Murdoch 1986; Ives 1992b), or when the host population is regulated by other density dependent forces (Hochberg and Lawton 1990a).

Spatial mechanisms of density dependence dominate the literature on host-parasitoid interactions. One of the much-studied ways to create spatial density dependence is through behavioral aggregation of adult parasitoids. At an individual behavioral level, Casas (chapter 2) begins with the premise that much of what we consider as real in adult parasitoid foraging behavior may be the artifacts of laboratory experimental designs. Employing real examples, he points to four ways in which a field approach may provide an essential understanding of host foraging behavior by parasitoids: (1) identification of new and important behavioral processes; (2) verification of processes widely accepted as important; (3) testing of theories developed in the laboratory or through the use of models; and (4) production of a priority list of processes requiring study. He believes that new technologies may make many once-impossible field studies on parasitoids a reality, but that there will remain insurmountable difficulties associated with parasitoid fieldwork that may impede progress.

Once a host is located by a female parasitoid, a variety of behaviors may ensue. Studies on parasitoid population dynamics often overlook the decisions that must be made by adult females during oviposition, such as sex ratio and clutch size. The few studies investigating these have discovered diverse effects on population dynamics. According to Heimpel (chapter 3), what is missing from previous models is an interdependence of life-history parameters. Diverse biological parameters may be phenotypically associated, and because each on its own may affect parasitoid-host interactions, inclusion of more than one via positive or negative trade-offs may have complex effects on population dynamics. The possibilities are immense, and Heimpel limits analysis to trade-offs between clutch size (the number of eggs deposited per host) and adult parasitoid attack rate mediated by egg limitation. He finds that egg limitation weakens the negative relationship between clutch size and host density, and he calls for future models to incorporate intraspecific variability in clutch size. The classic approach of varying a single parameter at a time and observing its effects on dynamics can be quite misleading, both for within- and between-population comparisons. His approach is all the more pertinent because the life-history and behavioral parameters that determine the population dynamics predicted by his models are known to be highly variable not only among species, but also among individuals within the same species.

Casas’s empirical approach and Heimpel’s more theoretical one point to how easily we may be misled by contrived experiments and simplistic models. Bernstein (chapter 4) addresses this directly by evaluating the utility of mathematical models in resolving the fundamental question of parasitoid population biology: What stabilizes host-parasitoid population dynamics? He traces models from Thompson’s work in the 1920s to the present and highlights three apparent answers to this question: (1) sigmoidal functional responses; (2) mutual interference between adult parasitoids; and (3) spatial heterogeneity in parasitism. Bernstein’s historical approach lucidly illustrates the scientific process: The sigmoidal functional response was promoted as a potential stabilizing mechanism for about fifteen years, mutual interference has had its ups and downs over the past thirty years, and although spatial heterogeneity received particular attention in the mid-1980s to early 1990s, it now appears to be receiving less attention. The latter two mechanisms are still generally accepted as potential candidates as the magic missing piece needed to stabilize host-parasitoid models, thereby resolving the contrast between instability in models and persistence in nature. Dovetailing nicely with Casas’s and Heimpel’s chapters, Bernstein prescribes that the way forward is to look at the behavioral nuts and bolts behind these nebulous stabilizing mechanisms. He does not dismiss the modeling approach, but rather says that for the future, it should have more behavioral realism and be testable in the field.

Harrison and her colleagues have conducted the first field test of one of the classic phenomena predicted by mathematical theory: diffusion-driven instability. Harrison (chapter 5) discusses how a large body of theoretical work points to fairly distinct predictions of how predator-prey interactions may generate fixed spatial patterns in abundance. Models that include host and parasitoid movement as diffusion processes predict that when parasitoids disperse at greater rates than their hosts, it is possible for areas of high host abundance to arise, surrounded and constricted by a ring of high parasitism caused by dispersing parasitoids. Harrison and colleagues conducted manipulative field studies on the western tussock moth and members of its parasitoid assemblage to test this prediction. Their findings are strikingly consistent with the model predictions. Nonetheless, the models and reality differ in key ways, and more system-specific models need to be made to test whether the experiments do in fact show all of the ingredients needed to produce diffusion-driven spatial patterns. Harrison’s chapter gives a clear example in which a striking natural pattern was first observed (the persistence of a spatially restricted tussock moth outbreak), theory provided a potential explanation (the more rapid dispersal of parasitoids than hosts from the center of the outbreak), and experiments confirmed many of the theoretical requirements for diffusion-driven spatial patterns.

At a larger spatial scale than that considered by Bernstein and Harrison, Hastings (chapter 6) addresses the problem of how parasitoid populations spread through time. Specifically, he presents a biologically simple model for parasitoid diffusion over a landscape and is able to arrive at a simple formula for the rate of parasitoid spread, employing information only about the per capita rate of population increase and rate of movement. He presents five case studies for which data are sufficient to say something about parasitoid spread. Interestingly, in three of the four studies where it could be determined, parasitoids spread tens of kilometers per year! In the remaining study, slow rates of spread may be a consequence of the parasitoid and host having been introduced into the habitat simultaneously; thus, Hastings concludes that the spread of the parasitoid is limited by the spread of its host. Hastings’s results are interesting because they provide indirect methods for assessing how individual movement rates translate into the overall rate of spread of the population. He suggests that movement studies combined with life-table analyses are a sensible way forward toward estimating the distance between the site of parasitoid emergence and where the parasitoids lay their eggs. In the future, Hastings’s approach could prove important both for understanding regional and geographical patterns in population dynamics and community structure, and for the employment of parasitoids in biological control.

How landscape patterns may affect parasitoid movement is discussed in detail by Roland (chapter 7). Over the past few years, Roland has designed an impressive series of experiments to uncover patterns in percent parasitism of the forest tent caterpillar over different spatial scales. Roland takes a landscape ecology perspective, explicitly focusing on the distribution of different types of habitat, both habitats containing forest tent caterpillars and habitats without. Roland points to three main features of landscapes: (1) composition, which is the characteristics of a given local habitat; (2) context, or the distribution of habitat types surrounding a local habitat; and (3) connectivity, which is determined by the global distribution of habitat types and how this distribution affects the ability of different parasitoids to navigate through the landscape. Roland argues that different features of landscapes affect different parasitoids in different ways, with each species experiencing landscape patterns at different spatial scales. Like Hastings, Roland calls for an integration of life-table studies with data on movement, but he concedes that this will be a difficult task to achieve.

Population Diversity

Parasitoids are distinguished from taxa employing other resource exploitation strategies by their astronomical diversity among just a handful of families. It goes without saying that phenomena hors norm attract the curious, and evolutionary biological approaches have been some of the most fruitful in explaining the diverse world of parasitoids (e.g., Godfray 1994; Quicke 1997). Although a large body of research is accumulating on the evolutionary biology and community structure of parasitoids, we are still far from the level of synthesis that is now possible in parasitoid population dynamics (see previous section).

Much work on parasitoid diversity has focused on how individual adult and larval parasitoid behavioral decisions percolate to determine structure at the population and community levels. Parasitoid behavior has many facets (Godfray 1994), conveniently divisible into adult search for hosts; oviposition on, in, or near hosts; and larval development on or within hosts. When behaviors and the population and community patterns to which they contribute are integrated over long time periods and/or over large spatial expanses, important patterns emerge (Hawkins and Sheehan 1994; Quicke 1997), such as host preferences and host range, niche partitioning with competing natural enemies, life-history strategies, and local adaptation and speciation.

At the behavioral level, there has been a renaissance over the past twenty-five years regarding how animals forage for resources that vary in space and time. Casas outlined how our field knowledge of foraging biology is still rudimentary, and Heimpel showed how the interdependence of search parameters could greatly affect population dynamics. Van Baalen’s premise (chapter 8) complements these two views on parasitoid behavior by considering how one should expect environmental conditions to determine fitness. Is the main determinant of parasitoid fitness the time the parasitoid has to search for hosts, or is it the number of eggs a parasitoid carries or can develop over its lifetime? Van Baalen suggests that a parasitoid’s biology should be molded through what amounts to gambling: In the face of an uncertain environment, a parasitoid must trade off investments in searching ability against investments in egg-laying potential, selecting the optimal trade-off to give the greatest chances of a big fitness payoff. Van Baalen employs a simple model to derive an explicit representation of parasitoid fitness. Analyzing this model, he finds that the optimal number of eggs a female parasitoid should carry depends both on the population densities of hosts and parasitoids and on the nature of their interaction, concluding that the optimal (evolutionarily stable) strategy is probably something intermediate between being limited by egg production and by the time available to search for hosts. Considered in a evolutionarily dynamic setting, populations may show cycles in the prevalence of time and egg limitation, indicating that a diversity of strategies may be maintained within a population. Van Baalen closes by highlighting the need for future studies on the evolution of gregariousness (as a mechanism for swamping the host’s immune system) and on host egg size (as a means of provisioning parasitoid juveniles in competitive environments).

An intriguing dichotomy in parasitoid life-history strategies is between koinobionts and idiobionts (Strand, chapter 10). Koinobionts generally attack mobile and growing host stages, thereafter usually developing endoparasitically over a prolonged period within the live host. In contrast, adult female idiobionts usually paralyze or kill immobile host stages (i.e., eggs and pupae), their larvae subsequently exploiting the host as an ectoparasitoid. Somewhat metaphorically, therefore, koinobionts are more akin to true parasites than to the more predatory strategy of idiobionts. Given that parasitoids exert strong selection pressures on their hosts to escape death, hosts should be expected to have a certain degree of latitude to combat each type of parasitoid according to its life history. For koinobionts, this may mean the evolution of physiological responses, the most studied being the primitive immune response called encapsulation. Godfray (chapter 9) gives a lucid presentation of the interest and importance of understanding the biology of parasitoid virulence (i.e., the ability of the parasitoid juvenile to develop to maturity) and host resistance (the ability to encapsulate parasitoid eggs). He discusses the theoretical advances in understanding host-parasitoid coevolution, most of this work occurring only in the last several years. Coevolutionary interactions can be usefully classified as graded or matching. Graded interactions are those in which on an absolute scale, some genotypes are better at either encapsulating eggs (host) or overcoming encapsulation (parasitoid). Matching interactions are those in which, to overcome host encapsulation defenses, the genotype of the parasitoid must match that of the host; no particular genotype for host or parasitoid is better, because the performance of the genotypes depends solely on the genotype of the opponent. Godfray suggests that graded interactions are probably more relevant to the process of encapsulation and provides empirical support for the prevalence of graded interactions. He calls for future work to examine in detail cellular dynamics, similar to that which has been done for vertebrate immune systems. It is quite possible that insect immune systems will shed unexpected light on those of vertebrates.

Godfray focuses on how reciprocal selection pressures could generate diversity in adaptations of parasitoids to exploit hosts and hosts to escape parasitoids. This is a micro-evolutionary problem. When considering cross-species comparisons of the evolution of life-history traits, one enters into the realm of macro-evolution. Strand’s thesis (chapter 10) is that developmental traits regulating parasitoid growth have been largely neglected as forces shaping parasitoid life histories. He begins by reviewing the two classic ways of understanding cross-species life-history variation: phylogeny and mode of host exploitation (exo- or endoparasitoid / idio- or koinobiont). He believes that failure to understand the developmental processes regulating life-history traits can lead to spurious conclusions about phylogenetic patterns. Strand presents a wealth of empirical studies showing that embryonic traits and the mode of parasitoid larval development have affected the direction of life-history evolution. He beckons for future studies to distinguish ecology and macro-evolution in shaping developmental traits.

A most fruitful way to integrate community structure has been to represent species ensembles in terms of their feeding relationships in the form of food webs. This perspective was pioneered in the 1960s, but for some reason, parasitoids seem to have missed out on food web models until only recently. Given the recurrent observation that many species, especially predators, feed at more than one trophic level, it is interesting that organisms as specialized as parasitoids are able to do so as well. Brodeur (chapter 11) presents a diversity of examples of parasitoids feeding in complex ways in food webs. He begins by investigating taxonomic patterns in the occurrence of hyperparasitoids, noting that (1) no parasitoid family consists uniquely of hyperparasitoids and (2) there are diverse lifestyles of hyperparasitism within any given clade, meaning that lower taxonomic scales are needed to understand the macro-evolution of this phenomenon. Brodeur then tackles the problems of hyperparasitoid host range and multitrophic interactions, concluding that even if some patterns are noticeable, much remains to be done. He calls for a better appreciation of the genesis of hyperparasitism, both as a biological strategy and as a macro-evolutionary process.

As does Brodeur, Holyoak (chapter 12) addresses issues involving parasitoid food chains; he tests the hypothesis that as parasitoids increasingly dominate communities, community food-chain length should decrease. This hypothesis is based on the following premises: (1) tightly coupled one predator-one prey interactions are more likely to produce unstable dynamics than diffuse many predator-many prey interactions; and (2) parasitoids have narrower prey ranges than predators. Thus, the greater instability of parasitoid-host food chains should limit their length relative to the more stable generalist predator-prey food chains. To investigate this prediction, Holyoak analyzes the patterns that appear when combining all fifty-eight available published food webs. He finds that there is a small but significant positive correlation between the proportion of enemies that are parasitoids and the number of species in the food webs—exactly the opposite of what was hypothesized. Although there is no relationship between the proportion of parasitoids and food-chain length, a very interesting pattern is revealed in terms of the distribution of species over trophic levels: In food chains with relatively more parasitoids than other natural enemies, fewer species occur at intermediate levels (3, 4, and 5) in the chain and more at the top levels (6 and 7). Holyoak points to the value of experimental manipulation in more powerfully resolving certain food web questions. He concludes, however, that we must ultimately rely on cross-web comparisons to assess the generality of pattern and process.

Holyoak’s premise is based on the cumulative destabilizing influence of tightly woven food chains. Another destabilizing force is interspecific competition within a trophic level. A central question for population biologists for almost a century has concerned the existence, nature, and strength of competitive interactions in ecological communities. One would think that if parasitoid assemblages are so speciose (with a mean of about five to six species per insect host species, but sometimes reaching more than one hundred), then they should be appropriate models for developing theories and conducting experiments and comparative analyses on competition. The problem is that competition may be idiosyncratically expressed in different macro-evolutionary periods, different communities, and different places. Therefore, detecting competition and extrapolating its importance should be done with caution. Hawkins (chapter 13) is aware of this. Using parasitoid assemblages, he searches for patterns that may reveal the impact of competition on community structure. There are many examples of strong competition between parasitoid species, particularly coming from biological control. Even though competition may be demonstrable within a community, however, the existence of competition does not necessarily imply that it affects the number and type of species in a community. By comparing local and regional parasitoid species richness, Hawkins finds scant evidence for the importance of competition to community structure. He explains this discrepancy using previous theoretical and empirical developments, which show that intense competition may be consistent with idiosyncratic patterns in vacant niches and with a lack of community saturation from local to regional levels. Hawkins suggests that although we can learn something about competition by following the intentional or serendipitous introduction of parasitoids into new geographical regions, we should be cautious about overinterpreting the results and applying them to natural, established communities.

Population Applications

Parasitoids have played a central role in the application of biological control (Hawkins and Cornell 1999). Indeed, many of the hundreds of studies modeling parasitoid population dynamics and diversity (see previous sections) have explicitly discussed applications to biological control (Mills and Getz 1996; Hochberg and Holt 1999). For the most part, these studies have focused on what ecological characteristics of host-parasitoid interactions contribute to the depression and stability of host (i.e., pest) populations. The major finding here is that greater stability of the interaction may sometimes come at a cost of less mean impact—and, therefore, less economic benefit—from biological control (e.g., Murdoch 1990).

A population biological perspective permits a scientific (i.e., repeatable and testable) means of understanding the successes and failures of natural enemies in biological control. Conversely, a better understanding of how biological control functions is not only desirable for basic research, but has also been championed as the most sensible way to conduct natural manipulative experiments toward a theoretical end (Hawkins and Cornell 1999). These manipulative experiments have two important caveats reducing their pertinence (at least for classical biological control, where an exotic parasitoid is imported for the control of an invading pest). First, exotic natural enemies do not necessarily have a long evolutionary history with the target host and the environment into which they are released. Therefore, they might not represent natural examples of parasitoid-host interactions. Second, biological control generally takes place in simplified ecosystems, such as agricultural crops or managed forests. Therefore, the environment in which parasitoid-host interactions take place may not be natural.

Taken together, these two caveats indicate that classical biological control introductions constitute unnatural testing grounds for population biological forces, and with less experimental control than would be the case in the more contrived cage experiments. It is our view, however, that if there is a science behind population biology, then it should be applicable to any kind of system, including the artificial systems of biological control.

Classical biological control can be broken down into a series of sequential steps, and each step can be analyzed using a population biological framework. The two principal steps Mills (chapter 14) distinguishes are establishment and impact. Establishment involves the following problems: How many parasitoids must be released? Where should they be released in the pest population? What sex ratio should be used? Should genetic variation be considered? Mills highlights the population dynamic phenomena of Allee effects, which require the initial density of released parasitoids to exceed a threshold for establishment to occur. He presents empirical evidence contrasting the effects on the establishment of host taxonomy, host refuges, parasitoid mating, landscape characteristics, climatic mismatch, and parasitoid founder effects. Turning to established parasitoid impact, Mills highlights the lasting depression of the pest population as the ideal. Three of the most important population approaches toward understanding impact in biological control are then discussed: spatial heterogeneity, parasitoid coexistence, and tritrophic interactions. Mills finds some evidence for each of these three factors to be related to impact in biological control, but it is far too early to draw any firm conclusions. He concludes that equilibrium-oriented theoretical approaches are not appropriate for understanding short-term dynamics. He calls for new approaches explicitly dealing with short-term dynamics, and for more dialogue between scientists and practitioners so that field testing becomes routine.

Tscharntke (chapter 15) considers agricultural landscapes as an unexpected habitat for conserving biological diversity. His applied view is surprisingly similar to Roland’s more fundamental one that spatial scale over landscapes sets the stage for population biological patterns. Tscharntke begins by drawing attention to how harsh agro-ecosystems really are for the component species; tillage, pesticides, fertilizers, and lack of vegetation diversification may all have adverse effects on parasitoids. In championing landscape aspects of agro-ecosystems, he focuses on vegetation adjacent to crop fields as parasitoid reservoirs. The idea is that cultivation perturbs parasitoid populations, and set-aside areas are necessary to create temporal and spatial bridges for the influx of parasitoids into the economically relevant arena. He presents substantial empirical evidence that the species composition and diversification of set-asides are important for parasitoids. In particular, he presents results that structural diversity of landscapes and the spatial distributions themselves are important to parasitism rates. Tscharntke predicts that landscape perspectives will be increasingly necessary in biological control, and they may even interact with other environmental perturbations, such as habitat destruction. He believes that generalizations will be impossible due to the unappreciated complexity of agricultural systems, but that the only way to build a scientific approach to understanding landscape effects on parasitoids is to start amassing well-conducted studies.

Although there are clear benefits to biological control, there are also risks. Effects of biological control agents on nontarget species is one of these. Even though candidate control agents are screened for possible nontarget effects, Roitberg (chapter 16) believes that type II errors (i.e., incorrectly accepting a null hypothesis, which, in this case, is no effect on nontargets) may permeate these screening programs. He argues that the complex reality of parasitoid behavior and the simplified laboratory methods used for assessing these behaviors are at the root of uncertainty in screening programs; this is very similar to Casas’s argument, but with an applied bent. Parasitoid effects on nontarget organisms can occur either if the parasitoids are not completely screened for all possible nontarget species, or if parasitoids evolve a broader host range following introduction. Roitberg argues that existing screening processes cannot assess the full host range likely to be adopted by parasitoids following release for biological control. He believes that evolutionary ecology provides a way to anticipate potential nontarget dangers based on life-history theory. Together with his colleagues, he has developed a series of dynamic life-history models to predict how life-history characteristics and environmental conditions influence the propensity of parasitoids to reduce host fidelity. Roitberg argues that host fidelity amounts to a complex surface of reaction norms (i.e., it is expressed differently in different environments), and therefore, evolutionary trajectories will be somewhat uncertain. It is the shape of host-fidelity reaction norms (steep, flat, linear, nonlinear) that provides an approach to guide practitioners in screening agents. Roitberg closes with a call for evolutionary biologists to take the bull by the horns and evaluate whether the ecological sciences have something to contribute to the predictability of nontarget effects.

Nontarget effects in biological control bring the specter of parasitoids threatening nontarget species with extinction. Hochberg (chapter 17) considers the converse problem—factors that threaten parasitoids with extinction. Given their immense diversity, it is reasonable to say that in terms of the number of species becoming extinct per unit time, we are losing more species of parasitoids than of any other type of insect. It is therefore perhaps somewhat puzzling that parasitoids have rarely been selected for conservation measures. Hochberg presents a number of values, in addition to biological control, that make parasitoids worthy of conservation measures. He also discusses how parasitoids may become endangered in the first place and prescribes rules of thumb that practitioners may use to develop conservation measures. Hochberg closes by presenting a case example of a detailed modeling approach to conserving rare parasitoids. The case involves an ichneumonid parasitoid, Ichneumon eumerus, which, although not appearing in the World Conservation Union’s IUCN Red Book of endangered species, should, since its unique host, the Lycaenid butterfly Maculinea rebeli, does. This is the most speculative chapter of the volume, but also appropriately serves as a final clarion call for more attention to noneconomic motives for the conservation of parasitoid biodiversity.

Conclusion

We echo the view of Hawkins and Sheehan (1994) that these are indeed exciting times for parasitoid ecologists, and more generally for parasitoid population biologists. However, we are also of the firm opinion that because recognition of the utility of parasitoids as biological models has really come to the fore only in the latter half of the 1900s, growth has been somewhat slow in terms of the number and diversity of research programs worldwide. One of our main objectives in this book is to communicate to interested young researchers that many questions, and even fields, are wide open to discovery using parasitoids as model systems.

¹ It is somewhat unfair to cast the problem as one developed only by Nicholson and Bailey, since it should be acknowledged that there were diverse earlier works, that of Thompson (1924) being the most relevant to the problem of parasitoids (see Mills and Getz 1996 for historical discussion). Recent years have also seen a recognition that models of host age-structure and of overlapping host-age classes can produce different dynamics to those cast in discrete, non-overlapping frameworks (i.e., Nicholson-Bailey models and their descendants) (see Briggs et al. 1999).

Part One

POPULATION DYNAMICS

Two

Host Location and Selection in the Field

JÉRÔME CASAS

MOST of what is known about the behavior and ecology of parasitoids has been discovered in the laboratory (Godfray 1994; Quicke 1997), and behavioral field studies of parasitoid species are rare (Waage 1983; Thompson 1986; Casas 1989; Janssen 1989; Driessen and Hemerik 1992; Connor and Cargain 1994; Visser 1994; Völkl 1994; Völkl and Kranz 1995; Heimpel et al. 1996, 1997; Völkl and Kraus 1996; Ellers et al. 1998; Henneman 1998). The lack of knowledge about host searching and host location in the field leads to two legitimate questions about (1) the importance, in the field, of the mechanisms studied in the laboratory and (2) the rationale in the choice of parameters in individual based models of host-parasitoid interactions (see Bernstein, chapter 4).

Foraging behavior in the field can be inferred indirectly from capture-recapture data and sampling of host and parasitoid populations. The information available by using this approach is on a time scale ranging from one hour to a generation. The processes of host finding and host selection occur on a much shorter time scale, however, typically of the order of minutes, and requires the direct observation of the foraging behavior of females.

In this chapter, I will identify three foraging parameters whose importance have been identified by conducting direct observations of foraging females in the wild. These parameters have been neglected in laboratory and theoretical studies so far. They are (1) the abundance of hosts as perceived by the parasitoid, (2) imperfect foraging cues, and (3) the time available for foraging. My arguments are developed by exploring in detail the few case studies in which parasitoids have been tracked continuously and their behavior recorded. Information about searching behavior in the field as observed in other, less studied, host-parasitoid systems is included when possible. It is my opinion that a deeper understanding of the foraging behavior of parasitic wasps will emerge through a comparative analysis of detailed case studies.

Sampling Rules and Host Abundance

A scientist’s sampling rules designed to obtain unbiased estimates of host density may be quite different from those used by foraging parasitoids. We know surprisingly little, except for the two examples described below, about the sampling rules used by parasitoids in the field, and how abundant hosts really are from the point of view of a parasitoid. In the first example, the parasitoid seems to have adopted a sampling strategy very well suited to the distribution of its host. In the second example, the low frequency of encounters with hosts leads to the acceptance of suboptimal hosts. Hence, both examples can be interpreted to show that perceived host abundance and distribution act as strong selection pressures on parasitoid traits related to host searching and host selection in the field. A third example shows how new knowledge about host density and host distribution in the field has changed our understanding of the patch leaving mechanisms of a parasitoid.

The moth Greya subalba (Lepidoptera: Incurvariidae) feeds within immature seeds of Lomatium dissectum (Umbelliferae) (Thompson 1987). The flowers are grouped into umbellets, commonly with five to fifteen flowers; these umbellets are, in turn, grouped into compound umbels of fifty to two hundred flowers. Until they mature, seeds are held together tightly in pairs, or a schizocarps. G. subalba females lay one—or less frequently, two—eggs per schizocarp, and the larva feeds within the immature schizocarp. Females tend to distribute their eggs broadly among umbellets, so that most umbellets have some larvae and the great majority of plants are attacked to some degree (25%–40% of seeds per plant are attacked). The distribution of attacked schizocarps among umbellets is well fitted by a truncated geometric distribution. The