Peter Stiling

How risky is biological control

The potential harmful effects of non—indigenous species introduced for biological control remain an important unanswered question, which we addressed by undertaking a literature review. There are few documented instances of damage to non—target organisms or the environment from non—indigenous species released for biological pest control, relative to the number of such releases. However, this fact is not evidence that biological control is safe, because monitoring of non—target species is minimal, particularly in sites and habitats far from the point of release. In fact, the discovery of such impacts usually rests on a remarkable concatenation of events. In addition to trophic and competitive interactions between an individual introduced species and a native one, many effects of introduced species on ecosystems are possible, as are numerous types of indirect interactions. Predicting such impacts is no mean feat, and the difficulty is exacerbated by the fact that introduced species can disperse and evolve. Current regulation of introduced biological—control agents, particularly of entomophages, is insufficient. At the very least, strong consideration should be given to the likely impact of both the pest and its natural enemy on natural ecosystems and their species, and not only on potential costs to agriculture, silvi—culture, and species of immediate commercial value.

Testing the enemy release hypothesis: a review and meta-analysis

One of the most cited hypotheses explaining the inordinate success of a small proportion of introduced plants that become pests is the ‘natural enemies hypothesis’. This states that invasive introduced plants spread rapidly because they are liberated from their co-evolved natural enemies. This hypothesis had not been properly tested until recently. Previous reviews on this topic have been narrative and vote counting in nature. In this review, we carried out quantitative synthesis and meta-analysis using existing literature on plants and their herbivores to test the different components of the enemy release hypothesis. We found supporting evidence in that (1) insect herbivore fauna richness is significantly greater in the native than introduced ranges, and the reduction is skewed disproportionally towards specialists and insects feeding on reproductive parts; and (2) herbivore damage levels are greater on native plants than on introduced invasive congeners. However, herbivore damage levels are only marginally greater for plants in native than in introduced ranges, probably due to the small numbers of this type of study. Studies quantifying herbivore impacts on plant population dynamics are too scarce to make conclusions for either comparison of plants in native vs introduced ranges or of co-occurring native and introduced congeners. For future research, we advocate that more than two-way comparisons between plants in native and introduced ranges, or native and introduced congeners are needed. In addition, the use of herbivore exclusions to quantify the impacts of herbivory on complete sets of population vital rates of native vs introduced species are highly desirable. Furthermore, three-way comparisons among congeners of native plants, introduced invasive, and introduced non-invasive plants can also shed light on the importance of enemy release. Finally, simultaneously testing the enemy release hypothesis and other competing hypotheses will provide significant insights into the mechanisms governing the undesirable success of invasive species.

Risks of species introduced for biological control

Numerous biological control introductions have adversely affected non-target native species. Although many of these problems occurred in the early days of biological control, some are recent. Because of how little monitoring is done on species, communities, and ecosystems that might be affected by biological control agents, it is quite possible that known problems are the tip of an iceberg. Regulations for officially sanctioned releases for biological control are insufficient, and there are also freelance unregulated releases undertaken by private citizens. Cost-benefit analyses for conservation issues, including those associated with biological control, are exceedingly difficult because it is hard to assign values to the loss of species or ecosystem functions. Risk assessment for biological control is difficult because of how hard it is to predict community- and ecosystem-wide impacts of introduced species and because introduced species disperse and evolve. Nevertheless, cost-benefit analyses and risk assessments for biological control introductions would have the salubrious effect of forcing consideration of myriad factors that now often receive cursory attention and of broadening public understanding of the issues.

The Frequency of Density Dependence in Insect Host-Parasitoid Systems

I examined case studies of density-related parasitism in insect host-para- sitoid systems reported in the literature. For 171 examples, the frequency of density de- pendence was 25% (n = 43), of inverse density dependence 23% (n = 39), and of inde- pendence 52% (n = 89). This is a considerably lower frequency of density dependence than previously reported in other reviews (Lawton and McNeill 1979, Lessells 1985, but see Dempster 1983). Biological features of case histories gave few clues as to the expected frequency of density dependence. Such features included host order, life stage attacked, parasite group, native vs. introduced status of hosts or parasites, number of attacking parasitoid species, mobile vs. sedentary hosts, and monophagous vs. polyphagous hosts or parasitoids. Biotic and abiotic factors may, however, provide good reasons for a low overall frequency of density dependence.

Non-additive effects of multiple natural enemies on aphid populations

The question of whether multiple natural enemies often interact to produce lower host mortality than single enemies acting alone has not yet been resolved. We compared the effects of four different combinations of natural enemies-parasitoids, predators, parasitoids plus predators, and no enemies-on caged aphid populations on marsh elder, Iva frutescens, in west-central Florida. Using starting densities of natural enemies commonly found in the field, we showed that parasitoid wasps reduced aphid population densities more than predatory ladybird beetles. The addition of predators to cages containing parasites reduced the ability of parasitoids to decrease aphid population densities. Because the experiments ran only over the course of one generation, such a reduction in the effectiveness of parasites is likely caused by interference of predators with parasitoid behavior. Parasitism in the cages containing both parasitoids and predators was reduced when compared to percent parasitism in parasitoid-only cages, but this could also be due to predation. Our experiments showed that ladybird beetles prey on parasitized aphids. Thus over the long-term, the effectiveness of parasites is impaired by the interference of predators on ovipositing parasitoids and by the predation of parasitized aphids. The effects of natural enemies in this system are clearly non-additive.

LOCAL ADAPTATION AND AGENTS OF SELECTION IN A MOBILE INSECT

The deme‐formation hypothesis states that selection can produce adaptive genetic variation within and among phytophagous insect populations. We conducted three field experiments and tested this prediction by transferring eggs and measuring performance of a mobile leafmining insect, Stilbosis quadricustatella. In Experiment 1, we compared the rate of mine initiation of leafminers transferred to natal and novel sites. In Experiment 2, we compared mine‐initiation rate of leafminers transferred to natal and novel host‐plant species. In Experiment 3, we compared the mine‐initiation rate, mine‐completion rate, and sources of mortality of miners transferred to neighboring natal and novel Quercus geminata trees. In the first, second, and third experiments, leafminer larvae initiated significantly more mines at the natal site, on the natal plant species, and on the natal Q. geminata tree, evidence for adaptive differentiation. Furthermore, plant‐mediated mortality was significantly lower among miners transferred to natal Q. geminata trees. This result supports a key assumption of the deme‐formation hypothesis: insects adapt to the defensive phenotypes of individual trees. However, natural‐enemy mortality was significantly higher among miners transferred to natal trees, essentially reversing the plant effect. Therefore, rates of successful mine completion were similar on natal (19%) and novel (17%) trees. This experiment suggests that host plants and natural enemies may represent opposing forces of selection. Leafminers adapted to individual trees may realize a selective advantage only when natural‐enemy densities are low.

DECREASED LEAF‐MINER ABUNDANCE IN ELEVATED CO2: REDUCED LEAF QUALITY AND INCREASED PARASITOID ATTACK

Most studies on the effects of elevated CO2 have focused on the effects on plant growth and ecosystem processes. Fewer studies have examined the effects of elevated CO2 on herbivory, and of these, most have examined feeding rates in laboratory conditions. Our study takes advantage of an open-top CO2 fertilization study in a Florida scrub-oak community to examine the effects of elevated CO2 on herbivore densities, herbivore feeding rates, and levels of attack of herbivores by natural enemies. Higher atmospheric CO2 concentration reduced plant foliar nitrogen concentrations, decreased abundance of leaf-mining insect herbivores, increased per capita leaf consumption by leafminers, and increased leafminer mortality. As suggested by other authors, reduced foliar quality contributed to the increase in herbivore mortality, but only partly. The major factor increasing mortality was higher attack rate by parasitoids. Thus increasing CO2 concentrations may reduce the survivorship of insect herbivores directly, by reducing plant quality, but also indirectly, by changing herbivore feeding and eliciting greater top-down pressure from natural enemies.

Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies

Resource quality (plant nitrogen) and resource quantity (plant density) have often been argued to be among the most important factors influencing herbivore densities. A difficulty inherent in the studies that manipulate resource quality, by changing nutrient levels, is that resource quantity can be influenced simultaneously, i.e. fertilized plants grow more. In this study we disentangled the potentially confounding effects of plant quality and quantity on herbivore trophic dynamics by separately manipulating nutrients and plant density, while simultaneously reducing pressure from natural enemies (parasitoids) in a fully factorial design. Plant quality of the sea oxeye daisy, Borrichia frutescens, a common coastal species in Florida, was manipulated by adding nitrogen fertilizer to increase and sugar to decrease available nitrogen. Plant density was manipulated by pulling by hand 25 or 50% of Borrichia stems on each plot. Because our main focal herbivore was a gall making fly, Asphondylia borrichiae, which attacks only the apical meristems of plants, manipulating plant nitrogen levels was a convenient and reliable way to change plant quality without impacting quantity because fertilizer and sugar altered plant nitrogen content but not plant density. Our other focal herbivore was a sap-sucker, Pissonotus quadripustulatus, which taps the main veins of leaves. Parasitism of both herbivores was reduced via yellow sticky traps that caught hymenopteran parasitoids. Plant quality significantly affected the per stem density of both herbivores, with fertilization increasing, and sugar decreasing the densities of the two species but stem density manipulations had no significant effects. Parasitoid removal significantly increased the densities of both herbivores. Top-down manipulations resulted in a trophic cascade, as the density of Borrichia stems decreased significantly on parasitoid removal plots. This is because reduced parasitism increases gall density and galls can kill plant stems. In this system, plant quality and natural enemies impact per stem herbivore population densities but plant density does not.

EXPERIMENTAL MANIPULATIONS OF TOP-DOWN AND BOTTOM-UP FACTORS IN A TRI-TROPHIC SYSTEM

There is much interest in assessing the relative importance of “top-down” (from the trophic level above) vs. “bottom-up” (from the trophic level below) effects in ecological communities. This study compares the strength of top-down effects of parasites and bottom-up effects of plants on herbivores. We established populations of sea-oxeye daisy, Borrichia frutescens, and gall-making flies, Asphondylia borrichiae, on 12 separate off-shore islands in Pinellas County, Florida (USA). High levels of parasitism were obtained by adding high densities of parasitized galls, and high levels of host-plant nitrogen were obtained by adding fertilizer. We established three replicates of each of the following treatments: low parasitism, low nitrogen; low parasitism, high nitrogen; high parasitism, low nitrogen; and high parasitism, high nitrogen. There was a significant interaction of parasitism and plant nitrogen: parasitism was important only on high-nitrogen plants where galls were abundant. Thus, our results contribute new insights into top-down vs. bottom-up effects: bottom-up forces set the stage on which top-down forces may act.

SPATIOTEMPORAL VARIATION IN LEAFMINER POPULATION STRUCTURE AND ADAPTATION TO INDIVIDUAL OAK TREES

Stilbosis quadricustatella leafminers are microlepidopteran specialists of sand-live oak (Quercus geminata). These tiny moths produce one generation per year and have a parasitic life-cycle and long larval stage that develops entirely within a single oak leaf. Differences in host-plant age, phenotype, and phenology generate a coarse-grained, spatially heterogeneous environment for the leafminer population. Previous reciprocal trans- fers of leafminer eggs among mature oaks revealed that S. quadricustatella are locally adapted to individual oak trees. In this paper we use genetic markers and an extinction- recolonization experiment to explore further variation in leafminer population structure. Allozyme loci indicate significant interdemic genetic structure among recent colonists of new host trees, which weakens in the 10th generation and disappears by the 40th generation. In contrast, adaptive demic structure is evident by the 10th generation and is strong in the 40th generation, despite the potential for substantial intertree dispersal. We propose that host heterogeneity combined with leafminer fidelity to natal trees promotes divergent se- lection and rapid demic evolution on individual oaks, despite potentially high gene flow between the leafminers inhabiting them.