Introduction Of Exotic Natural Enemies Research Articles

Testing a modified version of the EPPO decision-support scheme for release of classical biological control agents of plant pests using Ganaspis cf. brasiliensis and Cleruchoides noackae as case studies

The 6/04 standard of the European and Mediterranean Plant Protection Organisation (EPPO) on the safe use of biological control is a decision-support scheme (DSS) for the import and release of biological control agents in Europe. It was recently developed by the Joint EPPO/International Organisation of Biological Control (IOBC) Panel on Biological Control Agents. The DSS can be used to assess the potential environmental impacts of biological control agents. It is valid for different types of biological control: classical and augmentative biological control of invertebrates, pathogens and weeds. However, the DSS is not yet widely implemented in Europe and, during preliminary trials, it was found that its broad range of usages could lead to some confusion or misunderstandings, as well as requiring unnecessary information in some cases. Thus, the scheme was modified to specifically assess classical biological control against plant pests, i.e. the introduction of exotic natural enemies of plant pests for establishment and long-term control. The new version of the scheme was then tested on two parasitoids that are presently being released in Europe, the figitid Ganaspis cf. brasiliensis against the spotted wing drosophila Drosophila suzukii and the mymarid Cleruchoides noackae against the Eucalyptus bronze bug Thaumastocoris peregrinus. Both parasitoids were successfully assessed with the new version of the DSS. No major issues were encountered during the assessments and most questions were answered with low levels of uncertainty. Both assessments concluded that the parasitoids were safe to release in the impact assessment areas, with positive impacts exceeding negative impacts. Suggestions for potential improvements are provided.

Natural Enemies and Biological Control of Stink Bugs (Hemiptera: Heteroptera) in North America.

Simple SummaryStink bugs are important pests of many crops in the US, including row crops, vegetables, and tree fruits and nuts. Most stink bug management relies on broad-spectrum, disruptive insecticides with high human and environmental risks associated with them. These issues and increasing pesticide resistance in stink bugs are forcing pest managers to explore safer and more sustainable options. Here, we review the natural enemies of stink bugs in the US, noting that the egg and the late nymphal and adult stages of stink bugs are the most commonly attacked by parasitoids, whereas eggs and young nymphs are the stages most commonly attacked by predators. The effectiveness of stink bugs’ natural enemies varies widely with stink bug species and habitats, influencing the biological control of stink bugs across crops. Historically, biological control of stink bugs has focused on the introduction of exotic natural enemies against exotic stink bugs. Conservation and augmentation methods of biological control have received less attention in the US, although there may be good opportunities to utilize these approaches. We identify some considerations for the current and future use of biological control for stink bugs, including the potential for area-wide management approaches.Stink bugs comprise a significant and costly pest complex for numerous crops in the US, including row crops, vegetables, and tree fruits and nuts. Most management relies on the use of broad-spectrum and disruptive insecticides with high human and environmental risks associated with them. Growing concerns about pesticide resistance in stink bugs are forcing pest managers to explore safer and more sustainable options. Here, we review the diverse suite of natural enemies of stink bugs in the US, noting that the egg and the late nymphal and adult stages of stink bugs are the most commonly attacked by parasitoids, whereas eggs and young nymphs are the stages most commonly attacked by predators. The effectiveness of stink bugs’ natural enemies varies widely with stink bug species and habitats, influencing the biological control of stink bugs across crops. Historically, biological control of stink bugs has focused on introduction of exotic natural enemies against exotic stink bugs. Conservation and augmentation methods of biological control have received less attention in the US, although there may be good opportunities to utilize these approaches. We identify some considerations for the current and future use of biological control for stink bugs, including the potential for area-wide management approaches.

Hidden Host Mortality from an Introduced Parasitoid: Conventional and Molecular Evaluation of Non-Target Risk.

Hidden trophic interactions are important in understanding food web ecology and evaluating the ecological risks and benefits associated with the introduction of exotic natural enemies in classical biological control programs. Although non-target risk is typically evaluated based on evidence of successful parasitism, parasitoid-induced host mortality not resulting in visible evidence of parasitism (i.e., nonreproductive effects) is often overlooked. The adventive establishment of Trissolcus japonicus, an exotic parasitoid of the introduced stink bug Halyomorpha halys, provides an opportunity to investigate the total impact of this parasitoid on target and non-target hosts in the field. We developed a new methodology to measure nonreproductive effects in this system, involving a species-specific diagnostic PCR assay for T. japonicus. We applied this methodology to field-deployed eggs of four pentatomid species, coupled with traditional rearing techniques. Nonreproductive effects were responsible for the mortality of an additional 5.6% of H. halys eggs due to T. japonicus, and were even more substantial in some of the non-target species (5.4-43.2%). The observed hidden mortality of native non-target species from an introduced parasitoid could change predictions about direct and indirect ecological interactions and the efficacy of biological control of the target pest.

Possible coexistence of native and exotic parasitoids and their impact on control of Halyomorpha halys

Introduction of exotic natural enemies for biological control of invasive pests may disrupt existing ecological interactions, which may influence the outcome of biological control introductions. The interactions between Asian egg parasitoids, proposed as classical biological control agents of the highly polyphagous invasive pest Halyomorpha halys (Stal), and parasitoids native to the introduced area are largely unknown. Therefore, adult and larval interspecific competition between the exotic Trissolcus japonicus (Ashmead) and the European Anastatus bifasciatus (Geoffroy) was assessed (1) by observing aggressive interactions between adults of the two species following parasitization and (2) by providing each parasitoid species with previously parasitized H. halys egg masses at various time intervals. The results suggest that T. japonicus and A. bifasciatus engage in counterbalance competition, with the former being a superior extrinsic competitor (egg guarding and aggressiveness) and the latter being a superior intrinsic competitor (successful development from multiparasitized eggs of all ages). We suggest that the presence of T. japonicus is unlikely to have a negative impact on A. bifasciatus, and that those two species can coexist and potentially act synergistically in the biological control of H. halys.

Present Status of <I>Maconellicoccus hirsutus</I> (Hemiptera: Pseudococcidae) in the Mariana Islands and Its Control by Two Fortuitously Introduced Natural Enemies

The mealybug Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), attacks ornamental and fruit crops in the Mariana Islands. Insecticides cannot penetrate the heavy layers of wax that protect the insect's body. We surveyed the mealybug's locally recruited natural enemies and their effects on its population on Guam, Rota, Saipan, and Tinian to assess the need for introduction of exotic natural enemies. We monitored population densities of M. hirsutus, those of its natural enemies, and parasitism rates for 3 yr, 2005-2007. Our surveys revealed the presence of two parasitoids, Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) and Allotropa sp. near mecrida (Walker) (Hymenoptera: Platygastridae), fortuitously introduced to the Mariana Islands with M. hirsutus. The predator Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) also was often found feeding on M. hirsutus. Population density of M. hirsutus was below the economic threshold at all locations. Rainfall seemed to affect mean numbers of M. hirsutus and mean numbers of eggs at some locations. On all four islands, the two parasitoids, complemented by the predator, were effectively controlling the M. hirsutus population. No evidence of hyperparasitism was recorded. Currently, economic damage by M. hirsutus is not a concern in the Mariana Islands, and additional parasitoids need not be introduced to control M. hirsutus.

Are exotic natural enemies an effective way of controlling invasive plants?

Classical biological control (the introduction of exotic natural enemies) is often advocated as a tool for managing invasive species. Here, we review the effectiveness of biocontrol and explore the factors that determine whether it is an appropriate response to the invasive species problem. Although there have been some successes, biocontrol is generally poorly evaluated and, in many cases, its impact is unknown. In particular, there is limited understanding of the nature of the invasive species problem and no clear targets against which 'success' can be gauged. In addition, exotic natural enemies could act as invasive species in their own right. To improve the role of biocontrol in invasive species management, we need a better ecological understanding of the impacts of both the biocontrol agents and the target invasive species.

Classical Biological Control: A Critical Review of Recent Programs Against Citrus Pests in Florida

Classical biological control is often considered a cornerstone of integrated pest management, although the introduction of exotic natural enemies can have unpredictable and wide-ranging impacts on native ecosystems. In this article, I question the wisdom of using the classical approach as an automatic first response to invasive pests. I critically evaluate some classical biological control programs recently implemented against invasive pests of citrus in Florida including: Lysiphlebia japonica Ashmead and Lipolexis scutellaris Mackauer (Hymenoptera: Aphidiidae) introduced against the brown citrus aphid, Ageniaspis citricola Logviniskaya (Hymenoptera: Encyrtidae) against the citrus leafminer, and Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) against the Asian citrus psyllid. I advance the following contentions: (1) Not all invasive pests are appropriate targets for the classical approach, especially those that lack natural enemies specific to, or effective against them. (2) Some invasive pests may be effectively controlled by generalist predators within a time frame similar to that required for evaluation of introduced parasitoids. (3) The contributions of native species are often ignored when postrelease evaluations focus on introduced species. (4) Parasitism is a highly apparent phenomenon in the field, while predation is less apparent and far more difficult to quantify, an empirical disparity that may generate an undue bias regarding the perceived importance of introduced parasites relative to indigenous predators in biological control. (5) Classical programs have immediate political appeal to agricultural sectors seeking quick solutions to new pest problems, and to the government agencies seeking to respond to their demands for action. Thus, funding incentives for research may be biased toward ‘rear and release’ classical programs and away from other, ecologically sound approaches to pest management such as conservation biological control. I conclude that classical programs are typically employed as a reflexive response to invasive pests, often without adequate evaluation of the pest as a potential, rather than automatic, target for this approach, and without prerelease surveys to document indigneous natural enemies. A classical program may be embarked on regardless of whether or not suitable candidate species for introduction can be identified, and often without objective postrelease evaluations. The net result is a prevailing tendency to underestimate the potential ecological resiliency of established insect communities to invasive pests.

Predators impairing the natural biological control of parasitoids

A well known case of ineffective natural biological control: the puzzling coexistence of the coffee leaf miner, Leucoptera coffeellum (Guérin-Mèneville), and its natural enemies was analyzed. Despite being a suitable prey to eight parasitoid species and three wasp species, all occurring simultaneously, the coffee leaf miner too often presents populations far above the damaging level for the coffee plantation. It is demonstrated that predatory wasps and parasitoids interact negatively, possibly because predatory wasps kill parasitized miner's larvae. In doing so, predatory wasps indirectly kill parasitoids, thereby impairing the efficacy of the natural biological control. It is warned that biological control programs should be based on knowledge of food web interactions, rather than simply on strategies involving introduction of exotic natural enemies.

Procedures and policies in the USA regarding precautions in the introduction of classical biological control agents

Classical biological control, the introduction of exotic natural enemies to control non‐indigenous insect pests and weeds, has been practised in the USA for over 100 years. To date, there have been no fully documented, substantial negative results, and many important insect pests and weeds have been successfully controlled. Over the past decade, concern about the safety of biocontrol agents has increased in line with concern for general health of the natural, native biota. This concern has focused primarily on endangered, threatened, and listed species of plants, but is broadening to include most other organisms. Scientists, administrators and others involved in the process have long recognized the need to ensure that natural enemies of weeds do not attack commercially or horticulturally important plants and to ensure that natural enemies of insects do not attack beneficial species. Procedures for testing the host specificity of the natural enemies of weeds in their area of origin, before shipment to the country of release, have been developed to quite high levels of reliability but there is need for further improvements. Further host‐specificity testing is often required in quarantine in the USA. The rigour of this system is helped by the fact that all applications for permission to introduce biocontrol agents are examined by an Inter‐agency Technical Advisory Committee for Biological Control of Weeds (TAGBCW) before import permits are issued by the relevant authority (USDA APHIS/PPQ). TAGBCW review includes study of research plans and of lists of host plants for testing host specificity; it also analyses and offers advice on potential conflicts of interest. A ‘TAGBCW’ could be recommended for the European Union. With regard to natural enemies of insect pests, there is relatively little need for host‐range testing of most parasitoids because these are generally co‐evolved and intimately related organisms that are restricted to one or a few host species. Concern about the potential impact of oligophagous predators on non‐target organisms has increased recently and is a developing field of research. Some operating procedures that involve safety are discussed. The import permit system in the USA is presented, and two suggestions for changes in European permit procedures are suggested. Past regulatory procedures for classical biological control in the USA are described, and the current situation is presented.

Biological control of exotic pests in Italy: recent experiences and perspectives1

In Italy, successful application of classical biological control began in the 20th century, when Berlese released the predator Rodolia cardinalis in 1901 and the parasitoid Encarsia berlesei in 1906. Later, the ‘inoculative’ method was applied many times, limiting the misuse of insecticides and therefore achieving very positive effects for both the agricultural economy and environmental protection. When the establishment of new natural enemies failed, some exotic pests continued to damage important crops, sometimes disrupting any possibility of applying Integrated Pest Management (IPM). In other cases, new associations between exotic pests and native natural enemies occurred spontaneously and the importation of new species was not necessary: when no broad‐spectrum plant protection products are applied, some palaearctic parasitoids, such as Diglyphus isaea, naturally control the imported American leafminers Liriomyza trifolii and L. huidobrensis and some native predators (mainly Orius spp.) often control the exotic western flower thrips Frankliniella occidentalis. However, the introduction of natural enemies from the area of origin of the exotic pest is often the only alternative to chemical insecticides. Since its introduction in 1979, the American Flatid, Metcalfa pruinosa, has been spreading annually into new areas of the Mediterranean, causing severe damage to many crops because none of the indigenous natural enemies are sufficiently effective. Therefore, only the introduction of exotic natural enemies, such as the parasitoid Neodryinus typhlocybae, may reduce the outbreaks.

Perspective on the Use of Exotic Natural Enemies for Biological Control of Pest Grasshoppers (Orthoptera: Acrididae)

A previous manuscript (Lockwood 1993) questioned the introduction of exotic natural enemies for control of grasshoppers that affect rangeland and agricultural crops. This article presents some opposite viewpoints on the use of classical biological control, grasshopper biology, economic impact, management tactics, the specific natural enemies either released or slated for release, environmental concerns, and the review of these programs before release. In many areas, full agreement is indicated with positions presented by Lockwood; however, major differences of opinion exist. We believe that there is no scientific basis for establishing the new terminology “neoclassical biological control,” so traditional terminology is retained. Data on the use of arthropods and pathogensin classical biological control (including use of exotic natural enemies for control of native pests) show that this approach to pest management has controlled important pest species, has been associated with few if any serious environmental problems, and is aviable technique that was endorsed by the National Academy of Sciences and others. Therefore, the notion that the introduction of exotic natural enemies is categorically inappropriate is not accepted, nor is the idea that increased federal regulation would necessarily improve natural enemy establishment, improve control success, or eliminate negative environmental side effects. Rather, it is felt that mandatory Environmental Assessments and Environmental Impact Statements would restrict implementation of classical biological control. The specific programs questioned by Lockwood (1993) were based on significant biological information, were reviewed thoroughly, and hold potential to provide long-term mitigation of a severe economic pest problem while reducing environmental risk linked with widespread pesticide application.

Biological control: challenges and opportunities

Biological control, the use of living organisms as pest control agents, has enjoyed varying popularity over the past century, but today is well established as an important component of integrated pest management. We examine some current challenges to the use of biological control and particularly to classical biological control, the introduction of exotic natural enemies. These include conflicts of interest (1) with the conservation of native species and (2) between agricultural lobbies. On a scientific level, we examine two debates over the ecological and genetic basis of successful control. The challenge of Murdoch et al . ( Am. Nat . 125, 344-366 (1985)) to the notion of stability in pest populations under biological control, reveals that the stabilizing mechanisms may differ between pest taxa with different patterns of spatial dynamics. With respect to the hypothesis of Hokkanen & Pimentel ( Can. Ent . 116, 1109 (1984)) on the better chances of ‘new associations’ in biological control, we present an analysis that reaches different conclusions. Finally, we discuss future prospects for the different approaches to biological control, and suggest that longterm control methods, such as introduction and inoculation, will be used increasingly in the future.