John D. Reeve

Host–parasitoid spatial ecology: a plea for a landscape-level synthesis

A growing body of literature points to a large-scale research approach as essential for understanding population and community ecology. Many of our advances regarding the spatial ecology of predators and prey can be attributed to research with insect parasitoids and their hosts. In this review, we focus on the progress that has been made in the study of the movement and population dynamics of hosts and their parasitoids in heterogeneous landscapes, and how this research approach may be beneficial to pest management programs. To date, few studies have quantified prey and predator rates and ranges of dispersal and population dynamics at the patch level—the minimum of information needed to characterize population structure. From host–parasitoid studies with sufficient data, it is clear that the spatial scale of dispersal can differ significantly between a prey and its predators, local prey extinctions can be attributed to predators and predator extinction risk at the patch level often exceeds that of the prey. It is also evident that populations can be organized as a single, highly connected (patchy) population or as semi-independent extinction-prone local populations that collectively form a persistent metapopulation. A prey and its predators can also differ in population structure. At the landscape level, agricultural studies indicate that predator effects on its prey often spill over between the crop and surrounding area (matrix) and can depend strongly on landscape structure (e.g. the proportion of suitable habitat) at scales extending well beyond the crop margins. In light of existing empirical data, predator–prey models are typically spatially unrealistic, lacking important details on boundary responses and movement behaviour within and among patches. The tools exist for conducting empirical and theoretical research at the landscape level and we hope that this review calls attention to fertile areas for future exploration.

BIOLOGICAL CONTROL OF OLIVE SCALE AND ITS RELEVANCE TO ECOLOGICAL THEORY

Various authors have suggested that aggregation at local areas that have relatively many pests is an essential feature of parasitoids that are successful biological control agents. This behavior is thought to stabilize the pest-parasitoid system, and stability is considered essential for control. Such aggregation, however, can also be destabilizing. Strong aggregation independent of pest density is stabilizing, but leads to high pest density. We propose two models incorporating parasitoid distribution that is independent of pest distribution. In model A the parasitoids are gamma distributed and this yields Mays (1978) negative binomial model. Stability requires strong aggregation (γ < 1). In model B the parasitoids are evenly distributed, which yields Nicholson and Baileys (1935) unstable model. Using data from Huffaker and Kennetts study of the olive scale and its two introduced parasitoids in California, we show that the parasitoids do not aggregate to areas of high pest density. By comparing the observed distributions of parasitized hosts with those predicted by models A and B, we show that the system almost always fits the model A with γ > 1, and in some instances fit or was close to model B. In only one case out of eight is γ < 1. These results suggest that the system may be unstable, and this is supported by the observed fluctuations in scale numbers and parasitism through time. We conclude that spatial aggregation by parasites is not an essential feature of successful biological control. It may also be that stability is not essential for control, alternatively we may have failed to detect the salient density-dependent mechanism.

Stability, Variability, and Persistence in Host‐Parasitoid Systems

Insect parasitoids are ubiquitous members of natural insect communities, as well as being important agents of biological control. Because of their economic importance and relatively simple life cycles, host-parasitoid systems have received much theoretical effort. In this essay, I first review the theory available for hostparasitoid systems, and in particular explore the effects of environmental variability, spatial subdivision, and migration. These factors are often thought to influence dynamics in the field, but until recently have not received much attention in theory. I then make some recommendations for empirical work that could assess the effects of these factors in the field, and especially how they influence the persistence (through time) of host and parsitoid populations. Using the unstable Nicholson-Bailey model (Nicholson and Bailey 1935) as a starting point, theory has sought mechanisms that stabilize its dynamics; the rationale is that stability should ensure the persistence of the host and parasitoid (an apparent feature of real systems, at least on large spatial scales). Many stabilizing mechanisms have been identified, including mutual interference among parasitoids (Hassell and Varley 1969), several types of parasitoid aggregation (Hassell and May 1973, 1974, May 1978, Hassell 1984, Chesson and Murdoch 1986), density-dependent parasitoid sex ratios (Hassell et al. 1983, Comins and Wellings 1985), and competition among parasitoid larvae (Taylor 1988a). However, Morrison and Barbosa (1987) have questioned the idea that stability leads to persistence, when the population is subject to environmental variability. They used a standard host-parasitoid model, the negative-binomial model (May 1978), and simulated a fluctuating environment by allowing parameters in the model to be random variables. They found that perilously low densities could arise even when the model was strongly stable. Although stability ensures that

Regulation of an Insect Population Under Biological-Control

California red scale is suppressed to very low densities by the parasitoid Aphytis melinus. The system also appears stable. We report on an experimental test of the hypothesis that stability is caused by a refuge for scale. In a grapefruit grove in southern California in 1984-1985, the bark in the interior part of the tree provided a partial refuge from parasitism. Scale were -100 times denser there than in the exterior of trees. In a field experiment, we removed Argentine ants from some blocks of trees to test whether (1) ants caused the refuge by interfering with Aphytis and (2) the expected reduction in scale density in the refuge would lead to an unstable interaction in the exterior. We also tested for density- dependent parasitism, host mutilation, and predation by analyzing data from samples and from scale placed in the field. The temporal variability of the scale was at the low end of the range recorded in field populations. The experiment provided some evidence in support of the refuge hypothesis. The population in the refuge fluctuated much less than that in the exterior. Ant exclusion led to increased parasitism and lower scale density in the interior, and to increased fluc- tuations in abundance in the refuge and exterior. However, these changes were relatively small and perhaps temporary, suggesting that (1) ants are not the main cause of the refuge and that (2) we did not reduce the refuge density enough to determine whether the system would go unstable in the absence of the refuge population. Parasitism, host mutilation, and predation rates on scale showed no temporal density dependence, either direct or delayed, though detection of such patterns is difficult. Possible alternative stabilizing mechanisms include size-dependent interactions between red scale and Aphytis.

Statistical problems encountered in trapping studies of scolytids and associated insects.

Traps baited with semiochemicals are often used to investigate the chemical ecology of scolytids and associated insects. One statistical problem frequently encountered in these studies are treatments that catch no insects and, thus, have zero mean and variance, such as blank or control traps. A second problem is the use of multiple comparison procedures that do not control the experimentwise error rate. We conducted a literature survey to determine the frequency of these two statistical problems in Journal of Chemical Ecology for 1990–2002. Simulations were then used to examine the effects of these problems on the validity of multiple comparison procedures. Our results indicate that both statistical problems are common in the literature, and when combined can significantly inflate both the experimentwise and per comparison error rate for multiple comparison procedures. A possible solution to this problem is presented that involves confidence intervals for the treatment means. Options to increase the statistical power of trapping studies are also discussed.

Biological control by the parasitoid Aphytis melinus, and population stability of the California red scale

(1) The California red scale, a citrus pest, is under successful biological control by its parasitoid Aphytis melinus. Scale abundance is relatively stable, in comparison to other insect populations, and the rate of change of total scale abundance is density dependent. (2) Using data from a lemon grove, we have examined the scale-Aphytis system for several potential stabilizing mechanisms. These were: (a) density-dependent parasitism by Aphytis, in which parasitism rates vary in response to changes in scale density through time, (b) density-dependent sex-ratios in Aphytis, where the proportion of female progeny is influenced by both scale and parasitoid density, and (c) a spatial refuge from parasitism. (3) No evidence was found for the first two mechanisms. Parasitism rates were influenced only by rainfall, while sex-ratio was not significantly affected by any of the variables examined. (4) Strong evidence exists for a refuge from parasitism, which may account for the apparent stability of the system.

Eye size and behaviour of day- and night-flying leafcutting ant alates

The morphology of insect eyes often seems to be shaped by evolution to match their behaviour and lifestyle. Here the relationship between the nuptial flight behaviour of 10 Atta species (Hymenoptera: Formicidae) and the eye size of male and female alates, including the compound eyes, ommatidia facets, and ocelli were examined. These species can be divided into two distinct groups by nuptial flight behaviour: those that initiate the nuptial flight during the day and those that initiate it at night. The most striking difference between day- vs night-flying alates was in ocellus area, which was almost 50% larger in night-flying species. Night-flying species also had significantly larger ommatidia facets than day-flying species. A scaling relationship was also found between compound eye area, facet diameter, and ocellus area vs overall body size. Detailed observations are also presented on the nuptial flight behaviour of a night- vs day-flying species, A. texana and A. sexdens , respectively. The pattern in A. texana is for a single large and precisely timed nuptial flight before dawn, while flights of A. sexdens last for several hours, beginning at midday. Further observations suggest that the timing of the nuptial flight in A. texana is easily disrupted by light pollution.

Foraging Behavior of Aphytis Melinus: Effects of Patch Density and Host Size

The influence of size and density of the California red scale (Aonidiella aurantii) on the behavior of the parasitoid Aphytis melinus was examined. Aphytis appears to employ a simple strategy of searching the same amount of time in patches of different host density, and as a result the same fraction of hosts was encountered at all host densities. Only the first few of the encountered hosts were actually parasitized, however, probably due to egg depletion. Different instars of the California red scale yielded Aphytis progeny of different size and sex ratios. Small hosts, such as the second instar, produced small Aphytis with a male—biased sex ratio. The third instar, a larger host, produced much larger Aphytis and a more balanced sex ratio. Perhaps because of its low quality, the second instar was parasitized at a lower rate than the third instar, in both the field and laboratory. Parasitism on second instars in the field was lower when third instars were abundant. Host size distribution may have significa...

Diffusion models for animals in complex landscapes: incorporating heterogeneity among substrates, individuals and edge behaviours

1. Animals move commonly through a variety of landscape elements and edges in search of food, mates and other resources. We developed a diffusion model for the movement of an insect herbivore, the planthopper Prokelisia crocea, that inhabits a landscape composed of patches of its host plant, prairie cordgrass Spartina pectinata, embedded in a matrix of mudflat or smooth brome Bromus inermis. 2. We used mark-release-resight experiments to quantify planthopper movements within cordgrass-brome and cordgrass-mudflat arenas. A diffusion model was then fitted that included varying diffusion rates for cordgrass and matrix, edge behaviour in the form of a biased random walk and heterogeneity among planthoppers (sessile vs. mobile). The model parameters were estimated by maximum likelihood using the numerical solution of the diffusion model as a probability density. Akaikes information criterion (AIC) values were used to compare models with different subsets of features. 3. There was clear support for models incorporating edge behaviour and both sessile and mobile insects. The most striking difference between the cordgrass-brome and cordgrass-mudflat experiments involved edge behaviour. Planthoppers crossed the cordgrass-brome edge readily in either direction, but traversed the cordgrass-mudflat edge primarily in one direction (mudflat to cordgrass). Diffusion rates were also significantly higher on mudflat than for cordgrass and brome. 4. The differences in behaviour for cordgrass-brome vs. cordgrass-mudflat edges have implications for the connectivity of cordgrass patches as well as their persistence. Higher dispersal rates are expected between cordgrass patches separated by brome relative to mudflat, but patches surrounded by mudflat appear more likely to persist through time. 5. The experimental design and diffusion models used here could potentially be extended to any organism where mass mark-recapture experiments are feasible, as well as complex natural landscapes.

Parasitism and generation cycles in a salt-marsh planthopper

1. In warm climates many insects exhibit discrete generations, in the absence of obvious factors that could synchronize their age structure. It has been hypothesized that parasitoid wasps might be responsible for these oscillations in the host age structure, known as generation cycles. 2. We examine the role of the parasitoid Anagrus delicatus in the dynamics of the salt-marsh planthopper Prokelisia marginata. In particular, we evaluate the hypothesis that Anagrus contributes to the formation of generation cycles in the hopper, in the subtropical climate of Florida. 3. Two kinds of evidence are presented