Biocontrol of Pests of Apples and Pears in Northern and Central Europe - 3. Predators

Predators of apple and pear pests in northern and central Europe and their use as biological control agents are reviewed. Many natural enemy species are specialized feeders and are able to respond to the population dynamics of particular pest species. The most oustandingly successful example of this is the use of phytoseiid mites, particularly Typhlodromus pyri , against phytophagous pest mites in apple. This mite management strategy is now widespread throughout European apple growing regions. Another example is the use of Anthocoris nemoralis against pear psyllids, Cacopsylla pyricola and C. pyri . Several groups of naturally occurring polyphagous predators, such as chrysopids, coccinellids, syrphids and spiders, also prey on a number of pest species in orchards, contributing generally to the reduction in pest populations. However, they are unlikely alone to prevent pest damage fully and reliably. In seeking biological control opportunities for a particular pest, these polyphagous natural enemies are unlikely to be a high priority. An exception, due to its abundance in orchards, is the common earwig, Forficula auricularia , although this predator may also cause some fruit injury. Another option to consider when reviewing possibilities for biological control in orchards is the introduction of biological control agents. The success rate of this approach, using arthropod predators to control pests of field crops, has been generally poor. Furthermore, mass production methods for predators are likely to be difficult and very costly. The biological supplies industry is constantly seeking culture techniques, largely for arthropod biological control agents of pests of protected crops. It is possible that some future advance may be relevant to orchards, though currently available predators do not appear promising. A careful economic appraisal of the feasibility of use of any potential biological control agent would be prudent before embarking on research.     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.     

Effects of Predator and Prey Dispersal on Success or Failure of Biological Control

Biological control, defined as the reduction of pest populations by natural enemies, is often a component of integrated pest management strategies. Augmentation of natural enemy numbers by planned releases is a common biological control method, the successes and failures of which have been extensively reviewed. The effectiveness of biological control is influenced by how populations of predators and prey (or hosts and parasitoids) disperse in patchy environments. Here, we address the question of whether such dispersal leads to beneficial or detrimental pest control outcomes by developing a simple predator-prey model with constant releases of natural enemies in a two-patch environment. Theoretical and numerical results for all possible cases indicate that population dispersal has significant effects on the persistence of pests. For some ranges of dispersal rates or parameter space, dispersal is beneficial for pest control measures but this is not so for other ranges when it is detrimental. Therefore, knowledge of pest and natural enemy dispersal is crucial for understanding the effectiveness of biological control in a patchy environment. Finally, the model is generalised for multi-patch systems.     

Constraints to the implementation of biological control in Sri Lanka

Sri Lanka is a tropical island with a rich diversity of arthropods, with many species of indigenous natural enemies of economic pests. However, no extensive island wide surveys have been carried out for natural enemies of major crop ecosystems and only a few of the indigenous natural enemies are reported useful for augmentation biological pest control by massive field releases of laboratory-produced insects. Most successful biological control programs on the island are importation (i.e. classical) biological control programs, where established exotic natural enemies control certain pest populations in valuable crops. There is growing interest in the use of native natural enemies in pest management, thus creating a need for intensive research on the ecology of indigenous natural enemies and development of infrastructure and technology to produce natural enemies for augmentation. This paper examines constraints and opportunities for implementation of biological control in Sri Lanka.     

Optimum timing for integrated pest management: Modelling rates of pesticide application and natural enemy releases

Many factors including pest natural enemy ratios, starting densities, timings of natural enemy releases, dosages and timings of insecticide applications and instantaneous killing rates of pesticides on both pests and natural enemies can affect the success of IPM control programmes. To address how such factors influence successful pest control, hybrid impulsive pest-natural enemy models with different frequencies of pesticide sprays and natural enemy releases were proposed and analyzed. With releasing both more or less frequent than the sprays, a stability threshold condition for a pest eradication periodic solution is provided. Moreover, the effects of times of spraying pesticides (or releasing natural enemies) and control tactics on the threshold condition were investigated with regard to the extent of depression or resurgence resulting from pulses of pesticide applications. Multiple attractors from which the pest population oscillates with different amplitudes can coexist for a wide range of parameters and the switch-like transitions among these attractors showed that varying dosages and frequencies of insecticide applications and the numbers of natural enemies released are crucial. To see how the pesticide applications could be reduced, we developed a model involving periodic releases of natural enemies with chemical control applied only when the densities of the pest reached the given Economic Threshold. The results indicate that the pest outbreak period or frequency largely depends on the initial densities and the control tactics.     

Accounting for differential success in the biological control of homopteran and lepidopteran pests

One of the strongest patterns in the historical record of biological control is that programmes targeted against lepidopteran pests have been far less successful than those targeted against homopteran pests. Despite fueling considerable interest in the theory of host–parasitoid interactions, biological control has few unifying principles and no theoretical basis for understanding the differential pattern of success against these two pest groups. Potential explanations considered here include competitive limitation of natural enemy establishment, the influence of antagonistic parasitoid interactions, generation time ratio, and gregarious parasitoid development. An analysis of the biological control record showed that on average six natural enemies have been introduced per pest for both pest groups, providing no evidence of a differential intensity of competition. Similarly, use of a discrete time host–parasitoid model showed that antagonistic interactions that are common among parasitoids of Lepidoptera should not limit the success of biological control as such interactions can readily be counteracted by host refuge breaking. A similar model showed that a small generation time ratio (coupled with a broad window of host attack) and gregarious development can facilitate the suppression of pest abundance by parasitoids, and both were found to be positively associated with success in the biological control record. Of the four explanations considered here, generation time ratio coupled with a broad window of host attack appears to provide the best explanation for the differential pattern of success.     

Habitat linkages in conservation biological control: Lessons from the land–water interface

Terrestrial landscapes, including those with embedded agroecosystems, are a mosaic of cover types varying in size. Creating or maintaining habitats that support natural enemy populations to combat agricultural pests is the primary method of conservation biological control. Non-crop habitats can be managed in an attempt to maximize the exchange of natural enemies with adjacent agroecosystems with the expectation that they will suppress damaging pest outbreaks. Despite this goal, current habitat management relying on natural enemy spillover into crops has been unreliably effective at reducing pest abundance or increasing crop yield. Furthermore, the expansion and intensification of agriculture and changes in global climate patterns threaten the foundations of conservation biological control in future agroecosystems. However, the aquatic–terrestrial interface offers a natural boundary similar to the one between agroecosystems and their neighboring non-crop habitats that can provide useful insights to the challenges facing growers. Research of the exchanges between water and land suggests general biological and physical processes that govern the movement of organisms between disparate habitats. We propose that like aquatic insects moving from water to land, natural enemy dispersal from non-crop donor habitats into recipient crop patches on the landscape is a function of (1) the production of natural enemies in the source habitat which establishes the abundance of organisms that can disperse, (2) how and why mobile natural enemies disperse themselves into neighboring recipient habitats, and (3) the configuration of donor and recipient habitats on the landscape. We suggest that conservation biological control practitioners can focus on these main components of natural enemy production and dispersal to predict the effectiveness of conservation biological control measures and guide their adaptation to future global change.     

Behavioral studies,molecular approaches,and modeling: Methodological contributions to biological control success

Modern biological control practitioners must increasingly demonstrate a level of rigor that can only be achieved through use of effective methodological tools such as modeling, behavioral studies and molecular approaches. The use of these technologies is maturing rapidly in biological control and makes tangible contributions to its success. Behavioral studies often uncover important aspects of biology that would otherwise be overlooked, such as the influence of pre-release handling on establishment success and the response of natural enemies to host-induced plant volatiles. Molecular approaches allow the identification and detection of genetically distinct populations of invasive pest species and their natural enemies, tracing the origin of invasive pest populations and compatible natural enemies, and development of improved recombinant natural enemies. Modeling enables theory and empirical observation to optimize agent selection and release, and to predict quantitative impacts on target and non-target populations. All three methodologies, particularly in combination, contribute to our understanding of the reasons for success and failure in biological control, and together with post-release validation studies build the foundations to improve the success of future biological control releases.     

A meta-analysis of crop pest and natural enemy response to landscape complexity

Many studies in recent years have investigated the relationship between landscape complexity and pests, natural enemies and/or pest control. However, no quantitative synthesis of this literature beyond simple vote-count methods yet exists. We conducted a meta-analysis of 46 landscape-level studies, and found that natural enemies have a strong positive response to landscape complexity. Generalist enemies show consistent positive responses to landscape complexity across all scales measured, while specialist enemies respond more strongly to landscape complexity at smaller scales. Generalist enemy response to natural habitat also tends to occur at larger spatial scales than for specialist enemies, suggesting that land management strategies to enhance natural pest control should differ depending on whether the dominant enemies are generalists or specialists. The positive response of natural enemies does not necessarily translate into pest control, since pest abundances show no significant response to landscape complexity. Very few landscape-scale studies have estimated enemy impact on pest populations, however, limiting our understanding of the effects of landscape on pest control. We suggest focusing future research efforts on measuring population dynamics rather than static counts to better characterise the relationship between landscape complexity and pest control services from natural enemies.     

Assessment of interspecific interactions among parasitoids on the outcome of inoculative biological control of leafminers attacking chrysanthemum

Indigenous natural enemies occur within field grown crops at varying densities dependent upon a variety of other biotic and abiotic parameters. This natural control often does not provide adequate suppression, which results in the application of other pest management solutions including augmentative biological control. When releasing mass-reared natural enemies into a backdrop of existing natural enemy populations, competitive interactions are likely to occur. To assess the influence of these interspecific interactions on the outcome of such biological control practices studies were conducted in a simulated, field cage grown, cut chrysanthemum production system. Competitive interactions of two commercially available parasitoids were studied both in terms of parasitoid-host population dynamics and the impact of interspecific interactions on crop quality at harvest. The parasitoids Diglyphus isaea and Dacnusa sibirica attacking the leafminer Liriomyza langei were used as the model insect system. Both parasitoids are cosmopolitan and are known to occur in many ornamental production areas. Treatment comparisons included single species releases with complimentary releases of both species either simultaneously or with 2-week time lags, as well as a no release control to measure the background effects of natural mortality. Conclusions drawn from results of population-level studies replicated within and among years were that levels of interspecific competition among parasitoid species were undetectable at leafminer densities typical of field-grown ornamental crops (low densities), and thus, the efficacy of one species released into a backdrop of potentially competing parasitoids did not negatively or positively affect the outcome of the augmentative biological control, nor was there a positive outcome; however, crop quality at harvest was influenced.     

Assessment of interspecific interactions among parasitoids on the outcome of inoculative biological control of leafminers attacking chrysanthemum

Indigenous natural enemies occur within field grown crops at varying densities dependent upon a variety of other biotic and abiotic parameters. This natural control often does not provide adequate suppression, which results in the application of other pest management solutions including augmentative biological control. When releasing mass-reared natural enemies into a backdrop of existing natural enemy populations, competitive interactions are likely to occur. To assess the influence of these interspecific interactions on the outcome of such biological control practices studies were conducted in a simulated, field cage grown, cut chrysanthemum production system. Competitive interactions of two commercially available parasitoids were studied both in terms of parasitoid-host population dynamics and the impact of interspecific interactions on crop quality at harvest. The parasitoids Diglyphus isaea and Dacnusa sibirica attacking the leafminer Liriomyza langei were used as the model insect system. Both parasitoids are cosmopolitan and are known to occur in many ornamental production areas. Treatment comparisons included single species releases with complimentary releases of both species either simultaneously or with 2-week time lags, as well as a no release control to measure the background effects of natural mortality. Conclusions drawn from results of population-level studies replicated within and among years were that levels of interspecific competition among parasitoid species were undetectable at leafminer densities typical of field-grown ornamental crops (low densities), and thus, the efficacy of one species released into a backdrop of potentially competing parasitoids did not negatively or positively affect the outcome of the augmentative biological control, nor was there a positive outcome; however, crop quality at harvest was influenced.     

Using life stage-structured matrix models to determine natural enemy:pest release ratios for augmentative biological control

Augmentative biological control (ABC) is crucial for the integrated pest management (IPM) of greenhouse pests. The proper calculation of natural enemy:pest release ratio (NEPRR) stands out among the various challenges of ABC. Often, most NEPRR calculations only take into account the predation/parasitism efficiency of natural enemies, while disregarding pest population growth capacity, population structure and/or economic thresholds. In a model system consisting of Trichogramma pretiosum Riley parasitizing eggs of Tuta absoluta (Meyrick) on greenhouse tomatoes, we investigated whether a stage-structured Lefkovitch matrix could be used to determine suitable NEPRRs. The results suggested that these matrix models can potentially provide more precise and realistic predictions of NEPRRs since they account for differential pest population growth over time as a response to natural enemy action. The matrix models could also allow us to choose an adaptable NEPRR based on parameters such as the period the grower wishes to keep the pest population below economic threshold.     

The effect of within-crop habitat manipulations on the conservation biological control of aphids in field-grown lettuce

Within-crop habitat manipulations have the potential to increase the biological control of pests in horticultural field crops. Wildflower strips have been shown to increase the abundance of natural enemies, but there is little evidence to date of an impact on pest populations. The aim of this study was to determine whether within-crop wildflower strips can increase the natural regulation of pests in horticultural field crops. Aphid numbers in plots of lettuce grown adjacent to wildflower strips were compared with those in plots grown in the absence of wildflowers. The presence of wildflower strips led to a decrease in aphid numbers on adjacent lettuce plants during June and July, but had less impact in August and September. The decrease in aphid numbers was greatest close to the wildflower strips and, the decrease in aphid numbers declined with increasing distance from the wildflower strips, with little effect at a distance of ten metres. The main natural enemies found in the crop were those that dispersed aerially, which is consistent with data from previous studies on cereal crops. Analysis and interpretation of natural enemy numbers was difficult due to low recovery of natural enemies, and the numbers appeared to follow changes in aphid abundance rather than being directly linked to the presence of wildflower strips. Cutting the wildflower strips, to remove floral resources, had no impact on the reduction in aphid numbers achieved during June and July, but decreased the effect of the wildflower strips during August and September. The results suggest that wildflower strips can lead to increased natural regulation of pest aphids in outdoor lettuce crops, but more research is required to determine how this is mediated by natural enemies and how the impact of wildflower strips on natural pest regulation changes during the growing season.     

Evaluation of natural enemies for biological control: A behavioral approach

The success of biological pest control has stimulated the development of analytical models that explore the dynamics of natural enemies and their hosts or prey. These models seek to identify those general characteristics o f the natural enemy, host or prey population that lead to economic pest control. Because the models are strategic in nature, they are of limited value in identifying the specific attributes of an effective biological control agent prior to its introduction. Empirically developed criteria have also been of limited predictive value because they too provide only general guidelines. Behavioral ecology and foraging and sexratio theories may be useful adjuncts to these approaches, by identifying the evolutionary constraints and thus helping to define better the attributes of an effective natural enemy.     

Temporal variability of aphid biological control in contrasting landscape contexts

Landscape complexity may provide ecosystem services to agriculture through the provision of natural enemies of agricultural pests. Strong positive effect of adjacent semi-natural habitats on natural enemies in croplands has been evidenced, but the resulting impact on biological control remains unclear. Taking into account the temporal dynamics of pest and natural enemies in agricultural landscapes provides better resolution to the studies and better understanding of the biological control service.In this study, the population dynamics of aphids and two groups of predators (coccinellid and carabid beetles) were examined. Insects were sampled in 20 wheat fields, surrounded by structurally simple and complex landscapes in Chilean central valley. Considering the whole sampling period, the diversity of aphids and natural enemies were similar in wheat crops surrounded by both types of landscapes, and the abundance of ladybirds was higher in crops in the complex landscapes. The dynamics of predators was more advanced in complex landscapes than in the simple ones, whereas the dynamics of aphids were similar in both types of landscape. Negative correlation between abundance of predators and aphid population growth rate in both landscape contexts were observed suggesting a control of the pest population by the predators. Different temporal patterns were observed in these correlations in the two landscape contexts, which suggests differences in the biological control related to the landscape composition.The present study shows that colonization of crops by natural enemies occurs sooner in structurally complex landscapes and suggests that this early colonization may facilitate an early and efficient control of aphid populations, nevertheless the biological control efficiency seems to be higher in structurally simple landscapes later in the season.     

Connecting scales: Achieving in‐field pest control from areawide and landscape ecology studies

Areawide management has a long history of achieving solutions that target pests, however, there has been little focus on the areawide management of arthropod natural enemies. Landscape ecology studies that show a positive relationship between natural enemy abundance and habitat diversity demonstrate landscape‐dependent pest suppression, but have not yet clearly linked their findings to pest management or to the suite of pests associated with crops that require control. Instead the focus has often been on model systems of single pest species and their natural enemies. We suggest that management actions to capture pest control from natural enemies may be forth coming if: (i) the suite of response and predictor variables focus on pest complexes and specific management actions; (ii) the contribution of “the landscape” is identified by assessing the timing and numbers of natural enemies immigrating and emigrating to and from the target crop, as well as pests; and (iii) pest control thresholds aligned with crop development stages are the benchmark to measure impact of natural enemies on pests, in turn allowing for comparison between study regions, and generalizations. To achieve pest control we will need to incorporate what has been learned from an ecological understanding of model pest and natural enemy systems and integrate areawide landscape management with in‐field pest management.     

The state of commercial augmentative biological control: plenty of natural enemies,but a frustrating lack of uptake

Augmentative biological control concerns the periodical release of natural enemies. In commercial augmentative biological control, natural enemies are mass-reared in biofactories for release in large numbers to obtain an immediate control of pests. The history of commercial mass production of natural enemies spans a period of roughly 120 years. It has been a successful, environmentally and economically sound alternative for chemical pest control in crops like fruit orchards, maize, cotton, sugar cane, soybean, vineyards and greenhouses. Currently, augmentative biological control is in a critical phase, even though during the past decades it has moved from a cottage industry to professional production. Many efficient species of natural enemies have been discovered and 230 are commercially available today. The industry developed quality control guidelines, mass production, shipment and release methods as well as adequate guidance for farmers. However, augmentative biological control is applied on a frustratingly small acreage. Trends in research and application are reviewed, causes explaining the limited uptake are discussed and ways to increase application of augmentative biological control are explored.     

Integrating biological and chemical controls in decision making: European corn borer (Lepidoptera: Crambidae) control in sweet corn as an example

As growers switch to transgenic crops and selective insecticides that are less toxic to natural enemies, natural enemies can become more important in agricultural pest management. Current decision-making guides are generally based on pest abundance and do not address pest and natural enemy toxicity differences among insecticides or the impact of natural enemies on pest survival. A refined approach to making pest management decisions is to include the impact of natural enemies and insecticides, thereby better integrating biological and chemical control. The result of this integration is a dynamic threshold that varies for each product and the level of biological control expected. To demonstrate the significance of conserved biological control in commercial production, a decision-making guide was developed that evaluates control options for European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), in sweet corn, Zea mays L., where the primary natural enemies are generalist predators. Management options are lambda-cyhalothrin (broad-spectrum insecticide), spinosad (selective insecticide), Trichogramma ostriniae (Peng and Chen) (Hymenoptera: Trichogrammatidae) (parasitoid), and Bacillus thuringiensis (Bt) sweet corn (transgenic variety). The key factors influencing thresholds for all treatments are the intended market, predator populations, and the presence of alternative foods for the predators. Treatment cost is the primary factor separating the threshold for each treatment within a common scenario, with the lowest cost treatment having the lowest pest threshold. However, when the impact of a treatment on natural enemies is projected over the 3-wk control period, the impact of the treatment on predators becomes the key factor in determining the threshold, so the lowest thresholds are for broad-spectrum treatments, whereas selective products can have thresholds > 6 times higher by the third week. This decision guide can serve as a framework to help focus future integrated pest management research and to aid in the selection of pest management tools.     

Using lower trophic level factors to predict outcomes in classical biological control of insect pests

Importation of exotic natural enemies for biological control of insect pests entails risks to the environment. Pre-release estimates of the likelihood of achieving successful control would be helpful in avoiding ineffective importations. Based on strong evidence of multi-trophic level interactions in terrestrial ecosystems, we tested whether variation in ecological and biological factors found at the plant and herbivore trophic levels (levels one and two) could be used to create a simple, empirically based formula, capable of estimating the probability of successful biological control against holometabolous insect pests. We constructed a database consisting of 828 records of biological control attempts against 91 pest insect species and used stepwise logistic regression to test whether five basic features of the ecosystem, crop, and pest (habitat type, crop use, pest order, pest feeding niche, and damage severity) were correlated with rates of successful control. Natural enemy characteristics were not included in the model. The final model included 10 significant independent variables, nine of which were two-way interactions; all five basic ecosystem features appeared in significant interactions. The model provided good estimates of historical success rates against pest species in the data set. In a further test, the model was able to correctly rank amenability to biological control for 10 pest species not included in the original data set. These results provide evidence that lower trophic level factors can be useful in the search for a predictive formula for biological control.     

Adaptive defense of pests and switching predation can improve biological control by multiple natural enemies

One of the most important questions in biological control is whether multiple natural enemies can provide greater suppression of agricultural pests than a single best enemy. Intraguild predation (IGP) among natural enemies has often been invoked to explain failure of biological control by multiple enemies, and classical theoretical studies on IGP have supported this view. However, empirical studies are inconclusive and have yielded both positive and negative results. We extend classical models by considering anti-predator behavior of pests and diet switching of omnivorous natural enemies, and examine their effects on pest control. We assume that the pest can adaptively allocate effort toward the specific defense against each predator, and that the omnivorous natural enemy can consume disproportionately more of the relatively abundant prey (switching predation) by type III functional responses to prey items. The model predicts that adaptive defense augments pests but favors introduction of multiple natural enemies for controlling pests if IGP is weak. In contrast, switching predation does not make pest control by multiple natural enemies advantageous as in classical studies, in the absence of adaptive defense. However, switching predation reduces the necessity of defense by the pest against the omnivore and offsets the effect of adaptive defense. Thus, it makes the introduction of multiple natural enemies advantageous for pest control when the pest employs adaptive defense even if IGP is strong. These results suggest that types and combinations of behavior of prey and predators may greatly affect qualitative outcomes of biological control by multiple natural enemies.