The Impact of Resource Variation on Population Quality in Herbivorous Insects: A Critical Aspect of Population Dynamics

MaryCarol Rossiter    Department of Entomology, Pennsylvania State University, University Park, Pennsylvania

I. Introduction

A. The Relationship between Individual Quality, Population Quality, and Population Dynamics

B. Thesis and Organization of Chapter

II. Relevance of Population Quality to Population Dynamics

A. General Systems Theory Perspective

B. Support for Inclusion of Population Quality in Models of Population Dynamics

III. Criteria for Measurement of Population Quality

A. Sources of Phenotypic Variation in Population Quality

B. Estimating Population Quality Parameters

C. The Time Scale for Measuring Population Quality

IV. Resource Variation Effects Population Quality

A. Relationship between Food Quality and Population Quality

B. Population Quality Shifts Associated with Density Changes

C. The Influence of Maternal Effects on Population Quality

V. The Presence of Time-Delayed Effects on Population Growth

A. The Maternal-Effects Hypothesis of Population Outbreak

B. Action of Maternal Effects from a General Systems Perspective

C. The Biology of Maternal Effects

D. Testing the Maternal-Effects Hypothesis

References

I Introduction

A The Relationship between Individual Quality, Population Quality, and Population Dynamics

An important, but often overlooked feature of population biology is that environmental variation does not affect an herbivore population per se. It affects the individuals that make up that population. The contribution of an individual to the response of the population (e.g., mortality or fecundity) is determined by the interaction of its genotype and the environment it encounters. In theoretical models, the cumulative phenotypic effect of gene-environment interactions is represented by the average response of the population to each environmental feature included in the model. The use of average response to characterize an interaction between herbivore and environment is parsimonious, concise, and practical. However, it may not be a realistic representation if the variation that contributes to the average response is, itself, the premise for alternative developmental histories that have an additional impact on population growth (or decline) not otherwise expressed in the model.

Gene-environment interactions are responsible for qualitative features of an individual (i.e., life history expression) and for qualitative features of a population (i.e., average life-history expression of the group). The form of the gene-environment interactions, captured by population quality variables, can provide explicit proximal causes for the population dynamics of a species as well as ultimate causes for the population dynamics by virtue of their ability to alter the nature of feedback loops between the herbivore population and its environment.

I shall use general systems theory (Milsum, 1968; Berryman, 1981) as the framework to demonstrate that population quality should be included in the development of population dynamics models, whether the goal is to uncover general ecological processes or predict the population growth of a particular species. In the absence of information on the nature (i.e., the underlying biological mechanism) of a population's variation in physiological and behavioral adjustments to resource variation, there may be a great reduction in the utility of parameters typically used in the prediction of herbivore population dynamics-population size (N) and a population's average response to resources or natural enemies (e.g., based on predator-prey, or host quality-fecundity relationships). In this chapter, I shall argue that population quality is a critical variable in the ecological and evolutionary fate of herbivore populations. By extension, population quality is critical to community composition and stability whenever an herbivore population has a significant effect on the fate of other species in the community.

To understand fully the impact of resource variation on the population dynamics of an herbivore and its position in the community, we need, first, to consider the impact of resource variation on the individual. This bottom-up approach argues strongly for the need to consider the basic biology of the organism (genetics, development, behavior) when developing hypotheses about population and community-level phenomena. Individual quality describes the effect of the environment on the expression of a genotype with respect to the success (i.e., fitness) of the individual or lineage. By extension, population quality describes the cumulative impact of individual quality on success (i.e., growth or decline) of a population. Quality does not imply superiority; it merely recognizes that individuals and populations can differ by virtue of innate constitution and experience.

Throughout the history of population studies, mathematical ecologists have stated their awareness of both the importance and the omission of population quality in describing and predicting the fate of populations (e.g., Berryman, 1981; Lomnicki, 1988; Getz and Haight, 1989). With respect to humans, the economist and Nobel laureate T. W. Schultz (1980) thinks the omission arises from a reliance on the quantitative theory of populations, owing considerably to Malthus who "could not have anticipated the substitution by parents of quality for quantity of children" (p. 18). In the study of insects, W. G. Wellington was insightful, and also humorously indignant, that individuals of a population were viewed merely as participants of a count and cast into uniformity, a condition emblazoned with the title "monolithic lump of protoplasm" (Wellington, 1977, p. 2).

Population quality has been slighted for good reason. First, it is not immediately clear what should be measured, that is, which gene-environment interactions alter the probability of survival or reproduction. Second, the effort required to characterize the interaction between environmental heterogeneity and population quality can be staggering (Montgomery, 1990). Fortunately, recent advances in biotechnology and statistical and computing capabilities make such characterization feasible, and the process will become more efficient as collaboration between the sciences of organismal biology and population biology increases (e.g., see Calow and Sibley, 1990).

B Thesis and Organization of Chapter

It is the aim of this chapter to demonstrate that the inclusion of population quality variables in models of herbivore population dynamics can improve their heuristic value and predictive power. This improvement will support the development of successful herbivore control programs that minimize environmental hazard and the development of conservation programs aimed at the preservation of a particular herbivore taxon or entire communities in endangered habitats.

To establish the importance of population quality in herbivore population biology, I have focused primarily on temperate forest insects that experience outbreak. In Section II, I describe the relevance of population quality to population dynamics in terms of general systems theory. This is followed by empirical information that highlights the pitfalls of omitting population quality factors in theoretical and empirical studies of population dynamics. In Section III, the criteria for measuring population quality are provided, followed by a discussion of the conceptual and logistic difficulties of such measurements. Section IV focuses on the contribution of resource variation to the expression of population quality. The resource emphasized is food quality, critical in its own right and often the mediator in other ecological and autecological forces on the herbivore. Environmentally-based maternal effects provide a most remarkable example of the influence of resource variation on population quality. Environmentally-based maternal effects occur when the environmental experience of the parent(s) produces a phenotypic alteration in the offspring. This phenomenon is documented for a number of herbivore species. In Section V, the logic used in the development of the Maternal-Effects Hypothesis of Outbreak is presented with theoretical and empirical support. The chapter ends with a general approach to testing the hypothesis.

II Relevance of Population Quality to Population Dynamics

A A General Systems Theory Perspective

General systems theory provides an excellent framework to investigate the dynamic features of herbivore population behavior (see Berryman, 1981, 1989). To explain the participation of population quality in population dynamics, I shall apply the basic concepts of general systems theory (as outlined in Berryman, 1981) with a simple herbivore example. The components of the herbivore system represented in Figure 1 include...