Selecting arthropod biological control agents against arthropod pests: Can the science be improved to decrease the risk of releasing ineffective agents?

With greater emphasis being placed on management of the risks attached to natural enemy releases for biocontrol programs and the need to justify research budgets, the efficient selection of effective natural enemies is increasingly important. Historically there has been little agreement regarding how or whether this can be accomplished. Recent studies have demonstrated that there is good correspondence between insect host-finding behavior and attack rates in well-designed laboratory studies and their performance of this behavior in the field. Success in measuring efficacy of candidate agents remains somewhat of an art due to the multitude of factors influencing efficacy, but will be improved by attention to: (1) characterization of natural enemy candidates using morphological taxonomy or genetic markers at the onset of a program, (2) climatic matching candidate agents when possible, and (3) evaluations in semi-field or field cage conditions following quarantine evaluations whenever possible before proceeding with widespread releases. The application of these principles is discussed in regard to US biocontrol programs for Bemisia tabaci (Gennadius), Lygus spp., and Aphis glycines Matsumura. Proper project planning and interdisciplinary cooperation will enhance the chances for a successful project.     

The promotion of grassland forb abundance: A chemical or biological solution?

Techniques that increase the biodiversity value of species-poor grassland are required if conservation targets aimed at reversing the decline in species-rich grassland are to be met. This study investigated the diversification of swards dominated by Lolium perenne by testing the efficacies of two treatments applied to reduce competitive exclusion of species introduced as seed. The ‘biological’ treatment was the addition of the hemiparasitic plant species Rhinanthus minor, whilst the ‘chemical’ approach was the application of a selective graminicide, fluazifop-P-butyl (Fusilade 250EW). Changes in plant community composition were monitored for a period of 2 years. Values of plant species richness increased significantly between years regardless of treatment, but to a greater extent in plots sown with R. minor. The number of established sown species and their cover values were also significantly greater in association with R. minor. Fluazifop-P-butyl had no significant effect on species richness and tended to promote unsown species rather than those introduced as seed. Overall, the R. minor treatment was associated with the greatest impact on sward composition, facilitating establishment and development of the introduced species and promoting forb abundance.     

Increasing floral diversity for selective enhancement of biological control agents: A double-edged sward?

Floral resource subsidies can have differential effects on insect herbivores compared with the herbivores’ natural enemies. While the nectar of many plant species enhances parasitoid fitness, it may also increase damage by herbivores. This may occur as a result of enhanced herbivore fitness or by enhancing fourth-trophic-level processes, possibly disrupting a trophic cascade as a result. The responses of different arthropod guilds to different floral resource subsidies were compared using Plutella xylostella (Hyponomeutidae), its parasitoid Diadegma semiclausum (Ichneumonidae) and data from two other published herbivore–parasitoid systems. These were Dolichogenidea tasmanica (Braconidae) and its host Epiphyas postvittana, and Copidosoma koehleri (Encyrtidae) and its host Phthorimaea operculella. The parasitoids and hosts in the three systems exhibited differential responses to the nectar sources. The differential response was not explained by morphology, demonstrating that physical access to nectaries alone does not determine the potential of flowers as a food source. For some flowering plants, enhancement of herbivore and parasitoid fitness occurred. Other flowering plants, such as buckwheat and phacelia, conferred a selective enhancement on parasitoids by increasing only their fitness. More effective conservation biocontrol may be achieved by the provision of selective floral resources. Attempts to ‘engineer’ agroecosystems to enhance biological control require an extensive knowledge of the ecology of the herbivore, its enemies and their interactions with potential resource subsidies.     

Predicting population dynamics of weed biological control agents: science or gazing into crystal balls?

Abstract  Various factors can influence the population dynamics of phytophages post introduction, of which climate is fundamental. Here we present an approach, using a mechanistic modelling package (CLIMEX), that at least enables one to make predictions of likely dynamics based on climate alone. As biological control programs will have minimal funding for basic work (particularly on population dynamics), we show how predictions can be made using a species geographical distribution, relative abundance across its range, seasonal phenology and laboratory rearing data. Many of these data sets are more likely to be available than long-term population data, and some can be incorporated into the exploratory phase of a biocontrol program. Although models are likely to be more robust the more information is available, useful models can be developed using information on species distribution alone. The fitted model estimates a species average response to climate, and can be used to predict likely geographical distribution if introduced, where the agent is likely to be more abundant (i.e. good locations) and more importantly for interpretation of release success, the likely variation in abundance over time due to intra- and inter-year climate variability. The latter will be useful in predicting both the seasonal and long-term impacts of the potential biocontrol agent on the target weed. We believe this tool may not only aid in the agent selection process, but also in the design of release strategies, and for interpretation of post-introduction dynamics and impacts. More importantly we are making testable predictions. If biological control is to become more of a science making and testing such hypothesis will be a key component.     

Nematophagous fungi: prospective biological control agents of animal parasitic nematodes?

The rapidly escalating problem of anthelmintic resistance and the increasing concerns of chemical residues in livestock products and the environment pose serious threats to the future of chemotherapeutic control o f animal parasitic nematodes. One possible non-chemotherapeutic approach is biological control using nemotophagous fungi. Although Gr?nvold and colleagues recently described their experiments with two nematode-destroying fungi, Arthrobotrys and Duddingtonia, this alternate control option has received relatively little research attention. Here, Peter Waller broadens the discussion to consider the fundamental problems and prospects of this non-chemotheropeutic control strategy.     

A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.     

Does experimental evolution produce better biological control agents? A critical review of the evidence

Biological control of crop pests is considered a good alternative or complement to the use of pesticides. However, legislation restricts the importation of natural enemies of pests. A potential way to circumvent this limitation is by using experimental evolution and/or artificial selection to improve native biological control agents. Here, we review studies that have used these methodologies and evaluate their success. Experimental evolution or artificial selection has been used on a wide range of traits, with most focusing on improving the performance of natural enemies in ecologically relevant environments, such as in the presence of pesticides or at different temperatures. Although most studies were poorly replicated, the selected traits generally improved following the selection process. However, correlated responses (often in the form of trade‐offs) with other traits of interest were common. We suggest that the selection procedure can be improved by increasing replication and performing experimental evolution under more semi‐natural environments, to ensure that the most useful traits are being selected.     

Assessing the non-target impacts of classical biological control agents: is host-testing always necessary?

Release of a biocontrol agent in New Zealand is typically preceded by non-target testing of native or valued species. Nevertheless, if both the target pest and the natural enemy are very different from any native fauna, then there may be no scientific justification for host testing. Gonatocerus ashmeadi (Girault) (Hymenoptera: Mymaridae) is being considered as a biocontrol agent for glassy winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae), should the pest arrive. An assessment of the potential impact of G. ashmeadi on New Zealand’s Cicadellidae and Membracidae, from published literature data, indicates that none of these insects is at risk, as their eggs will not be recognised by the parasitoid because either their size or location places them outside the parasitoid’s search pattern. Consequently, there is no scientific case for any non-target host-testing to be carried out in containment.     

Native parasitic plants: Biological control for plant invasions?

Plant invasions cause biodiversity loss and degradation in ecosystems worldwide. The invasive species involved may be introduced, or native invaders, and controlling them is a major global challenge. Here, we highlight an emerging role for native parasitic plants in suppressing invasive species, thus aiding in restoration of affected habitats. Compelling empirical evidence is provided by three study systems located in Central Europe, southern Australia and eastern China. Further cases of parasitism of invasive plants have been recorded across five continents. We propose including the interactions between parasitic and invasive plants into the theoretical framework of the biotic resistance hypothesis concerning generalist interactions between invaders and native biota. Among parasitic plants, numerous root hemiparasites, mistletoes and parasitic vines show low host specificity and exert substantial negative effects on their hosts. These parasitic plants may interfere with key traits of invaders such as symbiotic nitrogen fixation or clonal propagation which provide them with competitive advantage over native species. We contend that some parasitic plants may present a cost‐effective environmentally sustainable component of invasion management schemes. Therefore, we encourage exploration of this potential and the development of methods for practical applications in ecological restoration and nature conservation.     

Is salinity an obstacle for biological invasions?

Invasions of freshwater habitats by marine and brackish species have become more frequent in recent years with many of those species originating from the Ponto‐Caspian region. Populations of Ponto‐Caspian species have successfully established in the North and Baltic Seas and their adjoining rivers, as well as in the Great Lakes–St. Lawrence River region. To determine if Ponto‐Caspian taxa more readily acclimatize to and colonize diverse salinity habitats than taxa from other regions, we conducted laboratory experiments on 22 populations of eight gammarid species native to the Ponto‐Caspian, Northern European and Great Lakes–St. Lawrence River regions. In addition, we conducted a literature search to survey salinity ranges of these species worldwide. Finally, to explore evolutionary relationships among examined species and their populations, we sequenced the mitochondrial cytochrome c oxidase subunit I gene (COI) from individuals used for our experiments. Our study revealed that all tested populations tolerate wide ranges of salinity, however, different patterns arose among species from different regions. Ponto‐Caspian taxa showed lower mortality in fresh water, while Northern European taxa showed lower mortality in fully marine conditions. Genetic analyses showed evolutionary divergence among species from different regions. Due to the geological history of the two regions, as well as high tolerance of Ponto‐Caspian species to fresh water, whereas Northern European species are more tolerant of fully marine conditions, we suggest that species originating from the Ponto‐Caspian and Northern European regions may be adapted to freshwater and marine environments, respectively. Consequently, the perception that Ponto‐Caspian species are more successful colonizers might be biased by the fact that areas with highest introduction frequency of NIS (i.e., shipping ports) are environmentally variable habitats which often include freshwater conditions that cannot be tolerated by euryhaline taxa of marine origin.     

Spontaneous Gac mutants of Pseudomonas biological control strains: cheaters or mutualists?

Bacteria rely on a range of extracellular metabolites to suppress competitors, gain access to resources, and exploit plant or animal hosts. The GacS/GacA two-component regulatory system positively controls the expression of many of these beneficial external products in pseudomonad bacteria. Natural populations often contain variants with defective Gac systems that do not produce most external products. These mutants benefit from a decreased metabolic load but do not appear to displace the wild type in nature. How could natural selection maintain the wild type in the presence of a mutant with enhanced growth? One hypothesis is that Gac mutants are "cheaters" that do not contribute to the public good, favored within groups but selected against between groups, as groups containing more mutants lose access to ecologically important external products. An alternative hypothesis is that Gac mutants have a mutualistic interaction with the wild type, so that each variant benefits by the presence of the other. In the biocontrol bacterium Pseudomonas chlororaphis strain 30-84, Gac mutants do not produce phenazines, which suppress competitor growth and are critical for biofilm formation. Here, we test the predictions of these alternative hypotheses by quantifying interactions between the wild type and the phenazine- and biofilm-deficient Gac mutant within growing biofilms. We find evidence that the wild type and Gac mutants interact mutualistically in the biofilm context, whereas a phenazine-defective structural mutant does not. Our results suggest that the persistence of alternative Gac phenotypes may be due to the stabilizing role of local mutualistic interactions.     

Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory?

Biological control of cyanobacteria is a well-researched area with a central focus on laboratory-scale studies. Numerous reports have been made on algicidal isolates, with bacteria as a major component of the antagonists. The research in this review draws a brief summary of what is currently known in the area of freshwater cyanobacteria being inhibited by bacterial isolates. Proteobacteria, Bacteroidetes and Firmicutes are among the most commonly reported phyla of bacteria associated with or employed in this research area. However, there are limited reports of upscaling these control measures beyond the laboratory scale. Lytic control agents are the most commonly reported in the literature with subsequent cyanotoxin release. From a water quality perspective, this is not feasible. Based on the available literature, temperature, pH and nutrient changes have been explored in this short review as possible contributors to less optimal bacterial performance. Moreover, the investigation into optimising some of these parameters may lead to increased bacterial performance and, therefore, viability for upscaling this biological control. Through the compilation of current research, this review offers insight to live predator-prey cell interactions between cyanobacteria and algicidal bacteria.

     

Alien futures: What is on the horizon for biological invasions?

Aim

To collect and identify the issues that may affect the future global and local management of biological invasions in the next 20–50 years and provide guidance for the prioritization of actions and policies responding to the management challenges of the future.

Location

Global

Methods

We used an open online survey to poll specialists and stakeholders from around the world as to their opinion on the three most important future issues both globally and at their respective local working level.

Results

The 240 respondents identified 629 global issues that we categorized into topics. We summarized the highest rated topics into five broad thematic areas: (1) environmental change, particularly climate change, (2) the spread of species through trade, (3) public awareness, (4) the development of new technologies to enhance management and (5) the need to strengthen policies. The respondents also identified 596 issues at their respective local working levels. Management, early detection, prevention and funding‐related issues all ranked higher than at the global level. Our global audience of practitioners, policymakers and researchers also elicited topics not identified in horizon scanning exercises led by scientists including potential human health impacts, the need for better risk assessments and legislation, the role of human migration and water management.

Main conclusions

The topic areas identified in this horizon scan provide guidance where future policy priorities for invasive alien species should be set. First, to reduce the magnitude and speed of environmental change and its impacts on biological invasions; second, to restrict the movement of potentially invasive alien species via trade; third, to raise awareness with the general public and empower them to act; and finally, to invest in innovative technologies that can detect and mitigate adverse impacts of introduced species.

     

What can DNA tell us about biological invasions?

It is often hoped that population genetics can answer questions about the demographic and geographic dynamics of recent biological invasions. Conversely, invasions with well-known histories are sometimes billed as opportunities to test methods of population genetic inference. In both cases, underappreciated limitations constrain the usefulness of genetic methods. The most significant is that human-caused invasions have occurred on historical timescales that are orders of magnitude smaller than the timescales of mutation and genetic drift for most multicellular organisms. Analyses based on the neutral theory of molecular evolution cannot resolve such rapid dynamics. Invasion histories cannot be reconstructed in the same way as biogeographic changes occurring over millenia. Analyses assuming equilibrium between mutation, drift, gene flow, and selection will rarely be applicable, and even methods designed for explicitly non-equilibrium questions often require longer timescales than the few generations of most invasions of current concern. We identified only a few population genetic questions that are tractable over such short timescales. These include comparison of alternative hypotheses for the geographic origin of an invasion, testing for bottlenecks, and hybridization between native and invasive species. When proposing population genetic analysis of a biological invasion, we recommend that biologists ask (i) whether the questions to be addressed will materially affect management practice or policy, and (ii) whether the proposed analyses can really be expected to address important population genetic questions. Despite our own enthusiasm for population genetic research, we conclude that genetic analysis of biological invasions is justified only under exceptional circumstances.     

Can ecological stoichiometry help explain patterns of biological invasions?

Several mechanisms for biological invasions have been proposed, yet to date there is no common framework that can broadly explain patterns of invasion success among ecosystems with different resource availabilities. Ecological stoichiometry (ES) is the study of the balance of energy and elements in ecological interactions. This framework uses a multi‐nutrient approach to mass‐balance models, linking the biochemical composition of organisms to their growth and reproduction, which consequently influences ecosystem structure and functioning. We proposed a conceptual model that integrates hypotheses of biological invasions within a framework structured by fundamental principles of ES. We then performed meta‐analyses to compare the growth and production performances of native and invasive organisms under low‐ and high‐nutrient conditions in terrestrial and aquatic ecosystems. Growth and production rates of invasive organisms (plants and invertebrates) under both low‐ and high‐nutrient availability were generally larger than those of natives. Nevertheless, native plants outperformed invasives in aquatic ecosystems under low‐nutrient conditions. We suggest several distinct stoichiometry‐based mechanisms to explain invasion success in low‐ versus high‐nutrient conditions; low‐nutrient conditions: higher resource‐use efficiency (RUE; C:nutrient ratios), threshold elemental ratios (TERs), and trait plasticity (e.g. ability of an organism to change its nutrient requirements in response to varying nutrient environmental supply); high‐nutrient conditions: higher growth rates and reproductive output related to lower tissue C:nutrient ratios, and increased trait plasticity. Interactions of mechanisms may also yield synergistic effects, whereby nutrient enrichment and enemy release have a disproportionate effect on invasion success. To that end, ES provides a framework that can help explain how chemical elements and energy constrain key physiological and ecological processes, which can ultimately determine the success of invasive organisms.