Arthropod Biological Control Research Articles

Metarhizium robertsii protease and conidia production, response to heat stress and virulence against Aedes aegypti larvae

Nutritional factors exert significant influence on the growth of entomopathogenic fungi, one of the main agents employed commercially in the biological control of arthropods. Thus, the objective of this work is to optimize the culture medium and solid fermentation time for production of proteases and conidia of Metarhizium robertsii ARSEF 2575 and to evaluate the interference of riboflavin and salts on virulence and resistance to abiotic stress factors. In the first step, nine groups were separated: negative control, positive control, and seven supplementation groups: ammonium nitrate, ammonium chloride, potassium nitrate, sodium nitrate, ammonium sulfate, ammonium phosphate, urea. Sodium nitrate showed significant difference in protease production at the time of 20 days of solid fermentation. Then, different concentrations of sodium nitrate and riboflavin as supplement were evaluated. Response surface methodology demonstrated that riboflavin and sodium nitrate influence proteolytic activity and conidia production, but without synergism. Supplementation of the medium with the optimal concentration of sodium nitrate and riboflavin did not interfere with the germination of conidia without exposure to abiotic stress, but did increase the thermotolerance of conidia. The presence of riboflavin and sodium nitrate at optimal concentrations in the culture medium did not alter fungal virulence with and without exposure to heat stress, varying according to the presence or absence of the supernatant during exposure, evidencing that resistance to heat exposure is multifactorial and dependent on intra- and extracellular factors. Moreover, the supplementation increased the larvicidal activity of the supernatant against Aedes aegypti.

Publisher Correction to: Integrating adverse effect analysis into environmental risk assessment for exotic generalist arthropod biological control agents: a three-tiered framework

Due to typesetting errors, Table 5 was not displayed correctly in the initial online publication. The original online article has been corrected.

Impact of heat stress on the development of egg and adult coccinellid Serangium japonicum: evidence for cross-stage and cross-generation effects

Arthropod biological control agents are at risk due to climate change, since heat stress negatively impacts their life history traits. Here, we investigated ontogenetic variation of thermal sensitivity in an important whitefly predator, Serangium japonicum Chapin (Coleoptera: Coccinellidae). In particular, we evaluated the impact of heat shock on survival rate, development, and reproduction of S. japonicum , and checked whether the negative effects resulting from heat stress are stage-related. The two most heat-tolerant stages of S. japonicum (egg and adult) were exposed to heat shock treatments at 36, 39, and 42 oC for 2 h, and 36 and 39 oC for 4 h. We found that heat shock significantly reduced egg-to-adult survival rate, extended egg-to-adult development time, and decreased fecundity and oviposition period compared to control (27 oC). The sex ratio however was not affected. Eggs exposed to heat shock led to adults whose weight and longevity were considerably reduced. The detrimental effects that resulted from heat shock were carried over to later life stages and even the next generation. Those carry-over effects were independent of stage except for egg-to-adult development time and adult weight. Our results suggest that releasing eggs or adults into fields or greenhouses makes little difference in reducing any negative impact on the developmental performance of S. japonicum induced by heat stress in a warming climate.

Exotic generalist arthropod biological control agents: need to improve environmental risk assessment to ensure safe use

Exotic generalist arthropod biological control agents (GABCAs) have been historically marginalized in classical and augmentative biological control due to their broad diet breadth, but an increasing demand for a more sustainable pest control is encouraging their reconsideration. This special issue compiles a collection of papers revealing that risks of several exotic GABCAs were overestimated, not all generalists are riskier than specialists and their environmental risk assessment (ERA) solely based on exposure analysis is inadequate. Three papers demonstrated that generalists were not involved in predicted non-target interactions: generalist idiobiont parasitoids probably do not exhibit interference competition with each other, an oligophagous exotic egg-larval koinobiont parasitoid does not compete with a native larval koinobiont, and an invasive generalist predator does not escape from its enemies. Two innovative methods for selecting non-target species are proposed, one based on existing food web data to predict indirect non-target effects, and the other on functional traits to predict competition with native natural enemies. Also a comprehensive GABCA-ERA method is proposed that integrates adverse effect analysis to the ‘conventional’ exposure analysis. The method was scrutinized by two studies: one suggesting that it could have resulted in faster and less costly decisions on two exotic generalists in New Zealand, and the other suggesting that eight exotic GABCAs released in Argentina might potentially reduce native natural enemies. We hope this special issue will stimulate the continued advance in the biosafety research of GABCAs so their safe use does not stagnate.

Integrating adverse effect analysis into environmental risk assessment for exotic generalist arthropod biological control agents: a three-tiered framework

Environmental risk assessments (ERAs) are required before utilizing exotic arthropods for biological control (BC). Present ERAs focus on exposure analysis (host/prey range) and have resulted in approval of many specialist exotic biological control agents (BCA). In comparison to specialists, generalist arthropod BCAs (GABCAs) have been considered inherently risky and less used in classical biological control. To safely consider exotic GABCAs, an ERA must include methods for the analysis of potential effects. A panel of 47 experts from 14 countries discussed, in six online forums over 12 months, scientific criteria for an ERA for exotic GABCAs. Using four case studies, a three-tiered ERA comprising Scoping, Screening and Definitive Assessments was developed. The ERA is primarily based on expert consultation, with decision processes in each tier that lead to the approval of the petition or the subsequent tier. In the Scoping Assessment, likelihood of establishment (for augmentative BC), and potential effect(s) are qualitatively assessed. If risks are identified, the Screening Assessment is conducted, in which 19 categories of effects (adverse and beneficial) are quantified. If a risk exceeds the proposed risk threshold in any of these categories, the analysis moves to the Definitive Assessment to identify potential non-target species in the respective category(ies). When at least one potential non-target species is at significant risk, long-term and indirect ecosystem risks must be quantified with actual data or the petition for release can be dismissed or withdrawn. The proposed ERA should contribute to the development of safe pathways for the use of low risk GABCAs.

Contributions to improve current environmental risk assessment procedures of generalist arthropod biological control agents (GABCAs) in Argentina

Argentina has over 100 years of experience in classical biological control, mostly based on the importation of biological control agents (BCAs) against arthropod pests. We present the state-of-the-art of the importation regulatory framework from the last 30 years to date. We also applied a part of a recent developed environmental risk assessment (ERA) methodology to analyze retrospectively the potential negative effects on non-target species of 15 BCAs (12 parasitoids and three predators) imported since 1996 in Argentina, supported by the published literature (Tier 1 Scoping Assessment and Tier 2 Screening Assessment). We demonstrated that the previously imported species could have negative effects on non-target species [Adverse Effect risk characterization > 5 for ERA categories 2 (Reduction of native natural enemies), 3 (Reduction in herbivory) and 4 (Reduction in valued species)], which would be worth evaluating with a Definitive Assessment (Tier 3) and field research to determine if any were actually occurring. We discuss some suggestions for government organizations, state officials and decision makers, scientific researchers, and biological control practitioners to improve the current evaluation for the introduction of new BCAs into Argentina.

Risk assessment procedures for biological control agents in New Zealand: two case studies for generalists

New Zealand’s indigenous and productive ecosystems are highly vulnerable to invasive species: therefore, New Zealand has stringent biosecurity legislation which encompasses the introduction of new biological control agents. To introduce a new agent, an application is made to the Environmental Protection Authority (EPA). The risk assessment carried out by the applicant is reviewed and a decision is made by an independent committee following public submissions and Māori consultation. An application will be declined if it is likely the new agent will cause significant adverse impacts on any indigenous species within its natural habitat, on natural habitats or on New Zealand’s inherent genetic diversity. Contrasting case studies are presented on two generalist arthropod biological control agents, one for a predatory mirid Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae) where the application was declined, and the other a predatory mite Neomolgus capillatus (Kramer) (Acarina: Bdellidae) which was considered for an application.

Challenges facing arthropod biological control: identifying traits for genetic improvement of predators in protected crops.

Biological control is an efficient pest control method but there are still limitations that are hindering its wider adoption. Genetic improvement of biological control agents (BCAs) can help to overcome these constraints, but the choice of key attributes for better performance that need to be selected is still an open question. Several characteristics have been suggested but the harsh reality is that selective breeding of BCAs has received a lot of attention but resulted in very little progress. Identifying the appropriate traits to be prioritized may be the first step to reverse this situation. In our opinion, the best way is to look at the factors limiting the performance of key BCAs, especially generalist predators (pesticide compatibility, prey-density dependence, non-suitable crops, and extreme environmental conditions), and according to these challenges, to choose the attributes that would allow BCAs to overcome those limitations. The benefits of selection for higher resistance to toxins, whether artificially applied (pesticides) or plant produced (plant defenses); increased fitness when feeding on non-prey food (supplemented or plant-derived); and better adaptation to extreme temperature and humidity are discussed. In conclusion, genetic improvement of BCAs can bring about new opportunities to biocontrol industry and users to enhance biocontrol resilience. © 2020 Society of Chemical Industry.

Ultrastructural and Cytotoxic Effects of Metarhizium robertsii Infection on Rhipicephalus microplus Hemocytes.

Metarhizium is an entomopathogenic fungus widely employed in the biological control of arthropods. Hemocytes present in the hemolymph of invertebrates are the cells involved in the immune response of arthropods. Despite this, knowledge about Rhipicephalus microplus hemocytes morphological aspects as well as their role in response to the fungal infection is scarce. The present study aimed to analyze the hemocytes of R. microplus females after Metarhizium robertsii infection, using light and electron microscopy approaches associated with the cytotoxicity evaluation. Five types of hemocytes (prohemocytes, spherulocytes, plasmatocytes, granulocytes, and oenocytoids) were described in the hemolymph of uninfected ticks, while only prohemocytes, granulocytes, and plasmatocytes were observed in fungus-infected tick females. Twenty-four hours after the fungal infection, only granulocytes and plasmatocytes were detected in the transmission electron microscopy analysis. Hemocytes from fungus-infected tick females showed several cytoplasmic vacuoles with different electron densities, and lipid droplets in close contact to low electron density vacuoles, as well as the formation of autophagosomes and subcellular material in different stages of degradation could also be observed. M. robertsii propagules were more toxic to tick hemocytes in the highest concentration tested (1.0 × 108 conidia mL−1). Interestingly, the lowest fungus concentration did not affect significantly the cell viability. Microanalysis showed that cells granules from fungus-infected and uninfected ticks had similar composition. This study addressed the first report of fungal cytotoxicity analyzing ultrastructural effects on hemocytes of R. microplus infected with entomopathogenic fungi. These results open new perspectives for the comprehension of ticks physiology and pathology, allowing the identification of new targets for the biological control.

Continental-scale suppression of an invasive pest by a host-specific parasitoid underlines both environmental and economic benefits of arthropod biological control

Biological control, a globally-important ecosystem service, can provide long-term and broad-scale suppression of invasive pests, weeds and pathogens in natural, urban and agricultural environments. Following (few) historic cases that led to sizeable environmental up-sets, the discipline of arthropod biological control has—over the past decades—evolved and matured. Now, by deliberately taking into account the ecological risks associated with the planned introduction of insect natural enemies, immense environmental and societal benefits can be gained. In this study, we document and analyze a successful case of biological control against the cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae) which invaded Southeast Asia in 2008, where it caused substantial crop losses and triggered two- to three-fold surges in agricultural commodity prices. In 2009, the host-specific parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) was released in Thailand and subsequently introduced into neighboring Asian countries. Drawing upon continental-scale insect surveys, multi-year population studies and (field-level) experimental assays, we show how A. lopezi attained intermediate to high parasitism rates across diverse agro-ecological contexts. Driving mealybug populations below non-damaging levels over a broad geographical area, A. lopezi allowed yield recoveries up to 10.0 t/ha and provided biological control services worth several hundred dollars per ha (at local farm-gate prices) in Asia’s four-million ha cassava crop. Our work provides lessons to invasion science and crop protection worldwide. Furthermore, it accentuates the importance of scientifically-guided biological control for insect pest management, and highlights its potentially large socio-economic benefits to agricultural sustainability in the face of a debilitating invasive pest. In times of unrelenting insect invasions, surging pesticide use and accelerating biodiversity loss across the globe, this study demonstrates how biological control—as a pure public good endeavor—constitutes a powerful, cost-effective and environmentally-responsible solution for invasive species mitigation.

Selecting non-target species for arthropod biological control agent host range testing: Evaluation of a novel method

Regulators often require risk assessment to ascertain biosafety of biocontrol agents before approval for release. Selecting the most informative non-target species for host range testing can be challenging. Here we compare traditional test list selection with a more objective method that selects species from a dataset of invertebrates from the receiving environment. A model, PRONTI (priority ranking of non-target invertebrates) ranks species using five criteria: hazard, exposure, potential ecological impacts from exposure, anthropocentric value and testability. For a case study, we used the braconid parasitoid Microctonus aethiopoides Loan released in New Zealand in 1982 for biocontrol of the pest weevil Sitona discoideus Gyllenhal. We compared species prioritised by PRONTI as worthy of testing with those selected prior to release. Several species which have been attacked in the field by M. aethiopoides since its release ranked highly suggesting that if PRONTI had been available pre-release, better predictions of non-target attack might have been made. The investment in time needed to adopt PRONTI needs to be balanced against its objectivity when comparing it with current conventional methods.

Mitigating the effects of insecticides on arthropod biological control at field and landscape scales

Integrated pest management (IPM) programs emphasize the combination of tactics, such as chemical and biological control, to maintain pest populations below economic thresholds. Although combining tactics may provide better long-term sustainable pest suppression than one tactic alone, in many cases, insecticides and natural enemies are incompatible. Insecticides can disrupt natural enemies through lethal and sub-lethal means causing pest resurgence or secondary pest outbreaks. Legislative actions such as the Food Quality Protection Act (US) and the Directive on Sustainable Use of Pesticides (EU) have placed greater restrictions on insecticides used in agriculture, potentially enhancing biological control. Here we focus on the effects of insecticides on biological control, and potential mitigation measures that can operate at different scales. At the farm scale, natural enemies can be conserved through the use of selective insecticides, low doses, special formulations, creation of refugia, special application methods, and targeted applications (temporal or spatial). At the landscape scale, habitat quality and composition affect the magnitude of biological control services, and the degree of mitigation against the effects of pesticides on natural enemies. Current research is teasing apart the relative importance of local and landscape effects of pesticides on natural enemies and the ecosystem services they provide, and the further development of this area will ultimately inform the decisions of policy makers and land managers in terms of how to mitigate pesticide effects through habitat manipulation.

Classical Biological Control for the Management of Alien Invasive Plants in Ireland

As a consequence of the sustained interest in exotic plants we now face the challenge of dealing with the economic and ecological impacts of many environmental weeds. Exotic ornamental plants can often flourish as they have been imported without their natural enemies that suppress the plant’s growth and reproduction in the native range. The aim of classical biological control is to re-establish the natural regulation provided by host-specific primary consumers from the native range of the weed. In contrast to the long history of arthropod biological control in Europe, environmental weed biological control is only now gaining some momentum. Ireland stands to benefit from developments made in other EU member states and other parts of the world as it shares many of the same environmental weed problems. Both terrestrial and aquatic weeds are good targets for biological control, and developments relevant to Ireland are described in this paper to illustrate the potential benefits of this management option.

Efficacy of spinosad bait sprays to control Bactrocera oleae and impact on non-target arthropods

A field study was conducted during 2005 and 2006 in Terra Quente, northeastern Portugal, to evaluate the efficacy of the spinosad-based insecticide Spintor Cebo® (Dow Agrosciences Iberica, S.A.) against the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), as well as the impact of the treatments on non-target arthropods. Results suggest that this insecticide could be as effective as dimethoate and since it was reported as having more benign toxicological and ecological profiles, it seems to be a good alternative to control the pest in Continental Mediterranean climates such as Terra Quente. However, its use should be evaluated carefully, mainly in conditions that increase the arthropod biological control agents’ propensity for feeding on it (e.g. absence of pollen, nectar and honeydews) to identify unintended impacts on conservation biological control of olive pests as a result of its application.

Benefits and risks of exotic biological control agents

The use of exotic (=alien) arthropods in classical and augmentative biological control programs has yielded huge economic and ecological benefits. Exotic species of arthropods have contributed to the suppression of key pests in agriculture and forestry or have aided in restoring natural systems affected by adventive species. However, adverse non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, e.g. 2% parasitization on a non-target insect on a local level, to massive effects on a large scale. Until now, no consensus on how to judge the magnitude of non-target effects and whether these effects can be tolerated or are unacceptable has emerged. In this paper, we briefly review both the benefits of biological control as well as the associated risks including to human and animal health, plant health and particularly the environment. We also make an attempt at identifying the major challenges for assessing risks and for balancing benefits and risks. There is general agreement that sound risk assessment procedures should precede the release of exotic invertebrate biological control agents and a recent shift—especially for arthropod biological control—from introductions done without meaningful risk assessment studies to projects conducting thorough host range testing can be observed. However, overly stringent regulations that would preclude promising agents from being developed must be avoided.

CLASSICAL BIOLOGICAL CONTROL FOR THE MANAGEMENT OF ALIEN INVASIVE PLANTS IN IRELAND

As a consequence of the sustained interest in exotic plants we now face the challenge of dealing with the economic and ecological impacts of many environmental weeds. Exotic ornamental plants can often flourish as they have been imported without their natural enemies that suppress the plant's growth and reproduction in the native range. The aim of classical biological control is to re-establish the natural regulation provided by host-specific primary consumers from the native range of the weed. In contrast to the long history of arthropod biological control in Europe, environmental weed biological control is only now gaining some momentum. Ireland stands to benefit from developments made in other EU member states and other parts of the world as it shares many of the same environmental weed problems. Both terrestrial and aquatic weeds are good targets for biological control, and developments relevant to Ireland are described in this paper to illustrate the potential benefits of this management option.

Effect of reduced risk pesticides on greenhouse vegetable arthropod biological control agents

Arthropod biological control agents (BCAs) are commonly released for greenhouse vegetable insect pest management. Nevertheless, chemicals remain a necessary control tactic for certain insect pests and diseases and they can have negative impacts on BCAs. The compatibility of some formulated reduced risk insecticides (abamectin, metaflumizone and chlorantraniliprole) and fungicides (myclobutanil, potassium bicarbonate and cyprodinil + fludioxonil) used, or with promise for use, in Canadian greenhouses with Orius insidiosus (Say), Amblyseius swirskii (Athias-Henriot) and Eretmocerus eremicus (Rose & Zolnerovich) was determined through laboratory and greenhouse bioassays. Overall, the insecticides and fungicides were harmless as residues to adult BCAs. However, abamectin was slightly to moderately harmful to O. insidiosus and A. swirskii in laboratory bioassays, whereas metaflumizone was slightly harmful to E. eremicus. In general, these products appear safe to use prior to establishment/release of these adult BCAs.

Evidence of alternative splicing of the chi2 chitinase gene from Metarhizium anisopliae

Metarhizium anisopliae is a filamentous fungus used in the biological control of arthropods and produces several chitinases in order to break the host cuticle chitin fibers. Chitinase function during fungal cell development and/or infection processes is also an important aspect when analyzing the life cycle of entomopathogens. The expression profile analysis of the endochitinase chi2 gene acquired by RT-PCR experiments indicated the presence of two different transcripts, suggesting the occurrence of alternative splicing in the chi2 gene. The presence of two transcripts, characterized by the removal or retention of the second 72 bp intron, was further confirmed by DNA sequencing, Northern blot and qRT-PCR. Furthermore, we detected the synthesis of two different proteins from the transcripts by two-dimensional Western blot and mass spectrometry analyses. This is the first reported occurrence of alternative splicing in M. anisopliae.

Florida's Established Arthropod Weed Biological Control Agents and Their Targets

ENY853, a 3-page fact sheet by J. P. Cuda and J. H. Frank, describes the role of biological control agents in controlling nonnative invasive weeds, lists the arthropod biological control agents that are established for seven invasive weeds, and provides links to additional resources. Includes references. Published by the UF Department of Entomology and Nematology, September 2009. ENY-853/IN779: Florida's Established Arthropod Weed Biological Control Agents and Their Targets (ufl.edu)

An analysis of historical trends in classical biological control of arthropods suggests need for a new centralized database in the USA

The documentation of biological control agents targeting arthropods in the United States has historically been subject to less regulation relative to weed biological control releases. This study reviews publicly available databases to track environmental releases of biological control agents targeting arthropods in the United States. It then presents available data for the states with the most releases between 1962 and 2005: Hawaii, California and Florida. These data indicate a clear decline in rates of introduction since 1982 or 1994, depending on the source. Existing record-keeping systems offer incomplete or inconsistent data for evaluation because they were designed with limited goals, attempt to capture excessive detail and are thus impractical, or are insufficiently resourced. Existing databases cannot be used to answer meaningful questions regarding non-target effects of introduced control agents. Current databases are inappropriately designed and insufficiently resourced to meet today's research and regulatory needs. We propose and describe a new database system for classical biological control of arthropods.