Estimating the relative roles of top-down and bottom-up forces on insect herbivore populations: a classic study revisited

Abstract

Although most ecologists agree that both top-down and bottom-up forces (predation and resource limitation, respectively) act in concert to influence populations of herbivores, it has proven difficult to estimate the relative contributions of such forces in terrestrial systems. Using a combination of time-series analysis of population counts recorded over 16 years and experimental data, we present the first estimates of the relative roles of top-down and bottom-up forces on the population dynamics of two terrestrial insect herbivores on the English oak (Quercus robur). Data suggest that temporal variation in winter moth, Operophtera brumata, density is dominated by time-lagged effects of pupal predators. By comparison, spatial variation in O. brumata density is dominated by host-plant quality. Overall, top-down forces explain 34.2% of population variance, bottom-up forces explain 17.2% of population variance, and 48.6% remains unexplained. In contrast, populations of the green oak tortrix, Tortrix viridana, appear dominated by bottom-up forces. Resource limitation, expressed as intraspecific competition among larvae for oak leaves, explains 29.4% of population variance. Host quality effects explain an additional 5.7% of population variance. We detected no major top-down effects on T. viridana populations. An unknown factor causing a linear decline in T. viridana populations over the 16-year study period accounts for most of the remaining unexplained variance. We discuss the observed differences between the insect species and the utility of time-series analysis as a tool in assessing the relative importance of top-down and bottom-up forces on herbivore populations.

Figure 1

The densities of (A) O. brumata and (B) T. viridana larvae on five Q. robur trees, sampled in Wytham Woods, Oxfordshire, from 1951 to 1966.

Figure 2

Log-transformed densities of (A) O. brumata and (B) T. viridana larvae on five Q. robur trees, sampled in Wytham Woods, Oxfordshire, from 1951 to 1966. The time–series for O. brumata is stationary, whereas the time–series for T. viridana exhibits a declining trend.

Figure 3

Mean log-transformed densities of T. viridana larvae on five Q. robur trees, sampled in Wytham Woods, Oxfordshire, from 1951 to 1966. The data have had the declining trend removed by transformation (see text for details) and points represent the mean of five trees.

Figure 4

Partial autocorrelation functions describing correlations between (A) O. brumata and (B) T. viridana larval densities at time t and densities at time t − 1, t − 2, … . t − 10. Note the dominant lag at t − 2 for O. brumata and t − 1 for T. viridana.

Figure 5

Regressions between the per capita rate of change of (A) O. brumata and larval density at time t − 2 and (B) T. viridana and larval density at t − 1. Because there is inherent autocorrelation in the regressions, probability estimates are presented for illustrative purposes only.

Figure 6

The relationship between the budburst date of individual Q. robur trees and the densities of (A) O. brumata and (B) T. viridana larvae in Wytham Woods, Oxfordshire. Data are reanalyzed from Hunter (29).

Figure 7

The relationship between the density of O. brumata larvae at time t − 1 and pupal predation at time t. Data for pupal predation, described as k5 from k-factor analysis, are from Varley et al. (21).