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.     

Trait-based approaches to predicting biological control success: challenges and prospects

Identifying traits that are associated with success of introduced natural enemies in establishing and controlling pest insects has occupied researchers and biological control practitioners for decades. Unfortunately, consistent general relationships have been difficult to detect, preventing a priori ranking of candidate biological control agents based on their traits. We summarise previous efforts and propose a series of potential explanations for the lack of clear patterns. We argue that the quality of current datasets is insufficient to detect complex trait–efficacy relationships and suggest several measures by which current limitations may be overcome. We conclude that efforts to address this elusive issue have not yet been exhausted and that further explorations are likely to be worthwhile.     

Delayed emergence and the success of parasitoids in biological control

Delayed emergence, a life history feature of many insects living in unpredictable environments, can have major consequences for the dynamics of host–parasitoid interactions, which vary according to their physiological interactions. We studied, through simple modeling, the significance of prolonged diapause on the suppression levels achieved by parasitoids and illustrate our case with a system involving a major forest pest, the woodwasp Sirex noctilio and two of its parasitoid species that have been introduced into different geographical regions through classical biological control programmes. Our findings suggest that the physiological relationship between parasitoid and host delayed emergence patterns may help understand observed variable success in several bio-control programs. We conclude that for given environments, host delayed emergence and the way in which parasitoids deal with it, should be included in the list of selection criteria of natural enemies of many pests, especially those affecting forests.     

Delayed emergence and the success of parasitoids in biological control

Delayed emergence, a life history feature of many insects living in unpredictable environments, can have major consequences for the dynamics of host–parasitoid interactions, which vary according to their physiological interactions. We studied, through simple modeling, the significance of prolonged diapause on the suppression levels achieved by parasitoids and illustrate our case with a system involving a major forest pest, the woodwasp Sirex noctilio and two of its parasitoid species that have been introduced into different geographical regions through classical biological control programmes. Our findings suggest that the physiological relationship between parasitoid and host delayed emergence patterns may help understand observed variable success in several bio-control programs. We conclude that for given environments, host delayed emergence and the way in which parasitoids deal with it, should be included in the list of selection criteria of natural enemies of many pests, especially those affecting forests.     

Classical biological control of ash whitefly: factors contributing to its success in California

The ash whitefly, Siphoninus phillyreae, invaded California in 1988 rapidly spreading throughout the state and infesting several species of ornamental trees and shrubs. Released Encarsia inaron rapidly established populations and spread throughout areas occupied by ash whitefly. We examined whether dispersal and overwintering ability could play a role in the extraordinary success of this parasitoid and we measured the impact of released parasitoids using a new method at a single location in northern California. The dispersal ability of E. inaron was examined by releasing two hundred and fifty adults 25 July 1991 into a single tree in a 1 ha pomegranate orchard near Brentwood, California. Based on yellow sticky card traps, the adult population spread at least 45 m from the release tree within 9 weeks of release. Over the same period of time the parasitoid population increased 64 fold. Impact was determined by measuring the number of ash whitefly adults produced in the absence and presence of E. inaron over 12 months. The production of whitefly adults, measured by the number of pupae entering the adult population, was reduced to very low numbers one year following the establishment of the parasitoid. Production of E. inaron adults increased rapidly, then decreased following the drop in production of ash whitefly adults. Duff of flowering pear trees was collected from under sample trees in mid winter to determine whether ash whitefly could survive on fallen leaves. Over fifty percent of adults emerged from whitefly pupae on leaves within 12 days of collection.     

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.     

Approaches to biological control problems

There has recently been some discussion as to the most effective methods of carrying out biological control investigations — the need for detailed ecological investigations, life-table studies, population studies, etc. This paper presents conclusions in this regard based on over 30 years experience in this field in many parts of the world. Often practical considerations make it impossible to carry out the long-term detailed ecological studies which would give a very valuable and scientifically interesting background to any biological control attempt before any introductions of beneficial species were made. Suggestions are made for the continuation of both short-and long-term procedures to be adopted in biological control work and examples cited of the value of both approaches.

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Résumé Quelques discussions ont eu lieu récemment concernant les méthodes les plus efficaces à appliquer dans les recherches sur la lutte biologique: nécessité d’investigations écologiques approfondies, études de tables de mortalité, études de populations, etc. Le présent article propose à ce sujet des conclusions fondées sur plus de 30 ans d’expérience dans de nombreuses parties du monde. Souvent, des considérations pratiques rendent impossibles les études écologiques à long terme, susceptibles d’apporter dans toute tentative d’application de lutte biologique, une connaissance de base scientifiquement très intéressante et très utile, préalablement à l’introduction d’organismes utiles. L’auteur suggère l’adoption simultanée, dans les travaux de lutte biologique, à la fois de la méthode à court terme et de la méthode à long terme; il cite des exemples de la valeur de ces deux stratégies.

     

Assessing the contributions of multiple interacting traits to plant reproductive success: environmental dependence

The reproductive success of sibling cocklebur plants (Compositae: Xanthium strumarium) was monitored after growth at different levels of availability of water and nutrient resources. Variation in reproductive success among individual plants was related to physiological, structural, and phenological characteristics. Reproductive success increased with increased availability of resources, but the relative contribution of particular traits to reproductive success varied with resource availability. Allocation of biomass to different vegetative tissues, time to seedling emergence, degree of branching, transpiration rates, water use efficiency, the rate of decline in height growth after seedling emergence and final plant size all varied significantly with resource availability. However, the changes in each of these phenotypic traits across three garden environments did not always correlate with reproductive success. The shifts across environments in the apparent importance of somatic traits for reproductive success were attributed to plastic changes in the traits but also to changes in the phenotypic correlations of the traits with reproductive success.     

Visual and somatosensory contributions to infant sitting postural control

Abstract

There are a limited number of studies that have investigated sitting posture during infancy and the contribution of the sensory systems. The goal of this study was to examine the effects of altered visual and somatosensory signals on infant sitting postural control. Thirteen infants (mean age?±?SD, 259.69?±?16.88?days) participated in the study. Initially, a single physical therapist performed the Peabody Developmental Motor Scale to determine typical motor development. Then the child was placed onto a force platform under four randomized conditions: (a) Control (C) – sat independently on the force plate, (b) Somatosensory (SS) – Sat independently on a foam pad (low density), (c) Visual (VS) – sat independently on the force plate while the lights were turned off creating dim lighting, and (d) Combination of b and c (NVSS). Center of pressure (COP) data from both the anterior-posterior (AP) and the medial-lateral (ML) directions were acquired through the Vicon software at 240?Hz. The lights off conditions, both VS and NVSS, lead to increased Root Mean Square (RMS) and Range values in the AP direction, as well as increased Lyapunov Exponent (LyE) values in the ML direction. Altered visual information lead to greater disturbances of sitting postural control in typically developing infants than altered somatosensory information. The lights off conditions (VS and NVSS), unveiled different control mechanisms for AP and ML direction during sitting. Thus, the present findings confirm the dominance of vision during the early acquisition of a new postural accomplishment.     

Mate finding, dispersal, number released, and the success of biological control introductions

Abstract.

• 1 An analysis of published data and a mathematical model of the population dynamics of introduced parasitoids were used to explore the possibility that biological control introductions fail because an Allee effect drives small, introduced populations extinct. Such an Allee effect would arise because low densities, resulting from dispersal into a new environment, lead to failure to mate, which leads to a male-biased sex ratio, which, if extreme enough, could cause population extinction.
• 2 For chalcidoids, ichneumonoids and tachinids, the proportion of parasitoid populations that established when introduced for control of lepidopteran pests increased with the number of parasitoids per release, the total number released, and the number collected when each variable was analysed separately. For chalcidoids alone, establishment increased with the number of releases for this variable analysed separately. However, stepwise logistic regression of establishment on these variables included only the total number released for chalcidoids and the number per release for ichneumonoids and tachinids. This suggests that an Allee effect may limit the establishment of introduced parasitoids more than stochastic environmental variation or lack of genetic variation.
• 3 A reaction-diffusion model of parasitoid introductions was developed, which included mate finding, dispersal, reproduction and survival. Sensitivity analysis showed that the critical number of females needed to establish a population decreased hyperbolically as mate detection distance and net reproductive rate were increased, but the critical number increased linearly as mean-square displacement was increased. The critical number of females did not change when the gross distance traversed per generation was varied. This was because increased area searched by males compensated for increased displacement. Changing from virgin females producing all males (arrhenotoky) to virgin females producing no progeny increased the critical number of females by over 30%.
• 4 The analysis of past introductions and the sensitivity analysis of the reaction-diffusion model both suggested a threshold of about 1000 insects per release to ensure establishment of introduced parasitoids. The implications of our results for the design of biological control introductions are discussed. Limitations in retrospective analyses and current knowledge indicate the need for an experimental approach to introductions.

     

Cryptic diversity,reproductive isolation and cytoplasmic incompatibility in a classic biological control success story

Molecular genetics and symbiont diagnostics have revolutionized our understanding of insect species diversity, and the transformative effects of bacterial symbionts on host life history. Encarsia inaron is a parasitoid wasp that has been shown to harbour two bacterial endosymbionts, Wolbachia and Cardinium. Known then as E. partenopea, it was introduced to the USA in the late 1980s from populations collected in Italy and Israel for the biological control of an ornamental tree pest, the ash whitefly, Siphoninus phillyreae. We studied natural populations from sites in the USA, the Mediterranean and the Middle East as well as from a Cardinium‐infected laboratory culture established from Italy, with the aims of characterizing these populations genetically, testing reproductive isolation, determining symbiont infection status in their native and introduced range, and determining symbiont role. The results showed that the two Encarsia populations introduced to the USA are genetically distinct, reproductively isolated, have different symbionts and different host–symbiont interactions, and can be considered different biological species. One (‘E. inaron’) is doubly infected by Wolbachia and Cardinium, while only Cardinium is present in the other (‘E. partenopea’). The Cardinium strains in the two species are distinct, although closely related, and crossing tests indicate that the Cardinium infecting ‘E. partenopea’ induces cytoplasmic incompatibility. The frequency of symbiont infection found in the native and introduced range of these wasps was similar, unlike the pattern seen in some other systems. These results also lead to a retelling of a successful biological control story, with several more characters than had been initially described.     

Evaluation of biogeographical factors in the native range to improve the success of biological control agents in the introduced range

Biogeographical factors associated with the invasive weed Arundo donax were evaluated at 22 different locations in four countries in its native range in reference to its key herbivore, an armoured scale insect, Rhizaspidiotus donacis. Data on climate, plant health and quality, soil conditions and anthropogenic influences were analysed for each site and compared to populations of R. donacis. Climate modelling from location data in Spain and France accurately predicted the native range of the scale in the warmer, drier parts of Italy and Greece and was used to predict its distribution in North America. Presence of the scale was not associated with specific soil type or characteristics. However, it was positively associated with a higher percentage of dead stems and significantly lower biomass of A. donax. Micronutrient sampling using leaf material found that sulphur was negatively correlated with aluminium and positively correlated with boron for scale density. Disturbance of field sites by cutting and/or addition of supplemental irrigation during summer appeared to disrupt the synchronised seasonal phenology of A. donax and R. donacis, leading to more robust stands. These biogeographical factors from the native range indicate that R. donacis should have the greatest impact in warm, dry climates in the introduced range where A. donax is undisturbed.     

Thermal plasticity and microevolution enhance establishment success and persistence of a water hyacinth biological control agent

Aspects of the thermal physiology of the water hyacinth biological control agent Eccritotarsus catarinensis Carvalho (Hemiptera: Miridae) have been extensively investigated over the past 20 years to understand and improve post‐release establishment in the field. Thermal physiology studies predicted that the agent would not establish at a number of cold sites in South Africa, where it has nonetheless subsequently established and thrived. Recently, studies have begun to incorporate the plastic nature of insect thermal physiology into models of agent establishment. This study determined whether season and locality influenced the thermal physiology of two field populations of E. catarinensis, one collected from the hottest site where the agent has established in South Africa, and one from the coldest site. The thermal physiology of E. catarinensis was significantly influenced by season and site, demonstrating a degree of phenotypic plasticity, and that some post‐release local adaptation to climatic conditions has occurred through microevolution. We then determined whether cold acclimation under laboratory conditions was possible. Successfully cold‐acclimated E. catarinensis had a significantly lower critical thermal minimum (CT_min) compared to the field cold‐acclimated population. This suggests that cold acclimation of agents could be conducted in the laboratory before future releases to improve their cold tolerance, thereby increasing their chance of establishment at cold sites and allowing further adaptation to colder climates to occur in the field. Although the thermal tolerance of E. catarinensis is limited by local adaptations to climatic conditions in the native range, the plastic nature of the insect's thermal physiology has allowed it to survive in the very different climatic conditions of the introduced range, and there has been some adaptive change to the insect's thermal tolerance since establishment. This study highlights the importance of plasticity and microevolutionary processes in the success of biological control agents under the novel climatic conditions in the introduced range.     

Biological control as an invasion process: disturbance and propagule pressure affect the invasion success of Lythrum salicaria biological control agents

Understanding the mechanisms behind the successful colonization and establishment of introduced species is important for both preventing the invasion of unwanted species and improving release programs for biological control agents. However, it is often not possible to determine important introduction details, such as date, number of organisms, and introduction location when examining factors affecting invasion success. Here we use biological control introduction data to assess the role of propagule pressure, disturbance, and residence time on invasion success of four herbivorous insect species introduced for the control of the invasive wetland plant, Lythrum salicaria, in the Columbia River Estuary. Two sets of field surveys determined persistence at prior release sites, colonization of new sites, and abundance within colonized sites. We quantified propagule pressure in four ways to examine the effect of different measurements. These included three measurements of introduction size (proximity to introduction site, introduction size at a local scale, and introduction size at a regional scale) and one measure of introduction number (number of introduction events in a region). Disturbance was examined along a tidal inundation gradient (distance from river mouth) and as habitat (island or mainland). Statistical models and model averaging were used to determine which factors were driving invasion success. In this study we found: (1) sparse evidence for the positive influence of propagule pressure on invasion success; (2) disturbance can negatively affect the invasion success of herbivorous insects; (3) the effects of disturbance and propagule pressure are species specific and vary among invasion stages, and (4) not all measures of propagule pressure show the same results, therefore single measures and proxies should be used cautiously.