Evolution and biological control

Biological weed control with pathogens: Search for candidates to applications

A survey of commercial producers and sellers of biological control agents revealed 49 species of invertebrate animals imported into Florida. Of these, 48 were imported for augmentative biological control of pests, and one for educational purposes. There were 3 species of nematodes, 1 mollusc, 8 mites, and 37 insects. More than half (25) of them were not known to occur in Florida at the time of importation, and some of them might be capable of establishing populations in Florida and might serve as classical biological control agents. Targets were mainly pest insects in the orders Homoptera (41%), Diptera (19%), Lepidoptera (15%) and Thysanoptera (11%). The targets were on or in perennial plants, annual plants, greenhouses, pasture- and turfgrasses, stored products, and feces of domesticated vertebrates. Some targets of commercially-imported biological control agents had been targets of classical biological control research. Some agents (@'common@') were imported frequently and by several producers, but others (@'uncommon@') were imported perhaps only once or twice. More targets previously recorded as targets of classical biological control agents were associated with @'uncommon@' commercially-imported agents than with @'common@' ones; more of the @'common@' agents than the @'uncommon@' ones were released into multiple habitats.

Current levels of suppression of waterhyacinth in Florida USA by classical biological control agents

Non-native invasive arthropod species threaten biodiversity and food security worldwide, resulting in substantial economic, environmental, social and cultural costs. Classical biological control (CBC) is regarded as a cost-effective component of integrated pest management programmes to manage invasive arthropod pests sustainably. However, CBC programmes are traditionally conducted once a pest has established in a new environment, and invariably all research needed to achieve approval to release a biological control agent can take several years. During that time, adverse impacts of the pest accelerate. A pre-emptive biocontrol approach will provide the opportunity to develop CBC for invasive pests before they arrive in the country at risk of introduction and therefore enhance preparedness. A critical aspect of this approach is that risk assessment is carried out in advance of the arrival of the pest. Implementing pre-emptive biocontrol risk assessment means that natural enemies can be selected, screened in containment or abroad and potentially pre-approved prior to a pest establishing in the country at risk, thus improving CBC effectiveness. However, such an approach may not always be feasible. This contribution defines the fundamental prerequisites, principles, and objectives of pre-emptive biocontrol risk assessment. A set of guidelines and a decision framework were developed, which can be used to assess the feasibility of conducting a pre-emptive risk assessment for candidate biological control agents against high-risk arthropod pests.

Eriophyoids are tiny plant-feeding mites belonging to the families of Eriophyidae, Phytoptidae and Diptilomiopidae. Eriophyoid mites are obligatory phytohages that infest all plant parts, except the roots. Most of them are quite host specific. About 80% of currently known recorded species of eriophyoid mites are associated with a single species of host plant. Classical biological control involves the introduction of control agents into a region, that does not form part of their natural area of distribution, to provide control of invasive weed species. In order to avoid direct damage to non target species, biological control agents must be highly host specific. Classical biological control of weeds depends on finding agents that are highly host-specific. Eriophyoid mites (EM) have long been thought to have high potential as biological control agents of classical biological control of weeds, and many review papers have emphasized their prospects. The use of phylogenies based on the statistical analysis of large numbers of characters, whether molecular genetic or morphological, can help traditional taxonomy and subsequently biological control. Correct systematic identification is a first step to finding prospective agents on the appropriate genotypes of the weed that are targeted for biological control.

In recent decades, the egg parasitoid Hadronotus pennsylvanicus (Ashmead) has gained substantial attention as an important natural enemy of pestiferous leaffooted bug species in the genera Anasa Amyot and Serville and Leptoglossus Guérin-Méneville. Throughout its native range of North America, H. pennsylvanicus parasitizes Anasa and Leptoglossus eggs in various vegetable and orchard systems. The overreliance on broad-spectrum insecticides in these systems and the demand for effective and sustainable coreid pest management strategies have motivated researchers to consider H. pennsylvanicus as an augmentative biological control agent. The potential use of H. pennsylvanicus as a classical biological control agent has also been studied in Europe in response to the rapid spread of Leptoglossus occidentalis Heidemann, an invasive pest causing significant economic losses to the European pine nut industry. Improved understanding of H. pennsylvanicus taxonomy, life history, host range, parasitoid–host ecology, laboratory rearing, and field deployment techniques have created a robust scaffold on which to build future biological control programs. This natural enemy profile reviews the current advances in the aforementioned areas of H. pennsylvanicus research and outlines the parasitoid’s prospects as a biological control agent.

To a large degree, the most serious insect and weed pests around the world are non-native, invasive species. Classical biological control, the introduction of natural enemies of invasive species to limit their populations, is a possible mechanism for alleviating the impacts of non-native pests. Whether introducing more non-native species in this way is a good approach depends on the positive and negative impacts of the potential control agents relative to the economic and environmental damage caused by the pests. Many classical biological control programs are deemed to be successful and contribute positively to ecosystem services by reducing the need for insecticides and herbicides as well increasing agricultural production, improving soil moisture conditions, and increasing native biodiversity. Recently, non-target impacts of some species of biological control agents have received considerable attention, which has impeded new classical biological control initiatives. However, analyses of the effectiveness of pre-release screening of agents shows that biological control has been very effective, particularly for weed control programs. Only 1–2 % of released agents have caused some damage to non-target species, and few have been shown to become invasive in the sense of being introduced, established, and having negative impacts in the new ecosystem. Clearly, generalist predators and parasitoids with multiple generations a year and multiple hosts should not be introduced because the potential for non-target impacts will be high. Host plant testing and specificity are important for choosing weed control agents, but must be viewed in the ecological context of species distributions and phenologies. However, the costs of lost opportunities from overly restrictive regulations must also be considered in evaluations of potential future classical biological control programs.

Biological control is considered the backbone of any integrated pest management programme. Exploring native ranges to identify new biological control agents is technically challenging and time-consuming; however, incorporating biogeographical insights into the selection process enhances the likelihood of success in biological control efforts. The zigzag beetle, Cheilomenes sexmaculata (F.), the most important and abundant of all ladybird beetles, feeds on a diverse range of prey. To study the population structure of C. sexmaculata, individuals were collected from five different zones, consisting of 25 subpopulations (subsets from their respective main zones) that uniformly represented India. We identified 109,585 contigs, 304,784 SNPs, and 46,583 INDELs, among which 5 INDELs and 9 SSRs were polymorphic. We observed high genetic diversity parameters for populations collected from the West Zone in all SNPs, SSRs, and INDELs markers. However, gene flow (Nm) was restricted, and FST was high in the South Zone and East Population (FST=0.45) populations, while the populations from the Central, North and West zones recorded zero FST. The structure and dendrogram construction analysis revealed individuals from Coorg and Mudigere of the South Zone and Barapani of the East Zone populations formed separate clusters. Mantel correlation revealed genetic distances decreased with the increasing geographical distance SNPs (Rxy= − 0.184 and P = 0.07); INDELs (Rxy= − 0.204 and P = 0.05) and SSRs (Rxy= − 0.339 and P = 0.06) indicated moderate genetic differentiation in the South and East zones populations due to geographic barriers, genetic drift and local environmental conditions. Populations in the North, West, and Central zones showed high gene flow, likely due to modern domestication and human activities. Additionally, the findings indicated that the populations from the West, North, and Central zones are better strains due to their high genetic fitness, so these populations can be used for classical and augmentative biological control.

Preliminary evaluation of the potential of the helminth parasite Rhabdias elegans as a biological control agent for invasive Puerto Rican coquís ( Eleutherodactylus coqui) in Hawaii

The ceutorhynchine weevilsHadroplontus litura(F.) andMicroplontus edentulus(Schultze) (Coleoptera: Curculionidae), are established in North America as biological control agents for Canada thistle,Cirsium arvense(L.) Scop., and scentless chamomile,Tripleurospermum perforatum(Mérat) M. Lainz (Asteraceae), respectively. In North America, both weeds occur sympatrically and in similar habitats as another ceutorhynchine,Ceutorhynchus obstrictus(Marsham) (cabbage seedpod weevil), an important pest of canola,Brassica napusL., andBrassica rapaL. (Brassicaceae). Ceutorhynchinae weevils released to control weeds in cultivated crops may serve as alternate hosts if agents released for biological control ofC. obstrictusare not specific to that species. Parasitoids associated withM. edentulusandH. liturainflict similar levels of mortality on their hosts, yet a single species was associated with the latter host, whereas 13 species attacked the former. The stem-miningM. edentulusappears to be at some risk but not the root-crown feedingH. litura, should the parasitoidsTrichomalus perfectus(Walker) andMesopolobus morys(Walker) (Hymenoptera: Pteromalidae) be introduced as biological control agents of the silique-feedingC. obstrictus. These findings suggest that feeding niche may be an important criterion for developing a nontarget species test list for host-range testing of potential biological control agents.

Classical biological control, i.e., the introduction of natural enemies from an invasive pest’s area of origin, has been proposed repeatedly to control the spotted wing drosophila Drosophila suzukii in the Americas and in Europe. Results from surveys in Asia and laboratory experiments suggest the parasitoid G1 Ganaspis cf. brasiliensis as a suitable biological control agent. To study the host specificity of the parasitoid under semi-field conditions, we conducted large-arena field cage releases. Parasitoids were released into cages at three dates in August 2021 in two regions of Switzerland. Released parasitoids had the choice to parasitize either D. suzukii larvae in fresh fruits (blueberries or elderberries) or the non-target native species D. melanogaster in decomposing fruits. The results were unequivocal in that apparent parasitism of D. suzukii larvae feeding in fresh fruits was on average 15%, whereas only one parasitoid emerged from D. melanogaster feeding on decomposing fruits (0.02% parasitism). Thus, the results support findings from previous laboratory experiments that G1 G. cf. brasiliensis is highly specific to D. suzukii larvae feeding in fresh fruits and parasitism of the closely related D. melanogaster feeding on decomposing fruits is very rare. Because in its invaded range, D. suzukii is the only Drosophila species that can attack and develop in undamaged fresh fruits, we conclude that open field releases of the parasitoid G1 G. cf. brasiliensis should not pose significant risks to non-targets.

7 Classical biological control of plant pathogens

Classical biological control in the past has been characterized by numerous unsuccessful attempts and by relatively few outstanding successes. An analysis of the recent developments in the theoretical and applied aspects of classical biological control reveals, however, that introducing parasites (predators, pathogens, herbivores) against pest organisms apparently has a considerable potential of solving or lessening many important pest problems of the world. In this review, classical biological control was found to be applicable everywhere in the world regardless of temperature or moisture conditions, and native pests were found to be as susceptible to biological control as introduced pests. Biocontrol success was found to be a function of several independent variables (e.g., characteristics of the pest and control organism and the target ecosystem) and many dependent variables (e.g., the methods of selecting, propagating, and introducing the control organism). Knowledge about the interactions between these factors and other, external factors, will help to find probable ways of improving the success rate in introducing natural enemies. This has already been demonstrated by the steady increase in the efficiency of biocontrol work in the last 30 to 40 years.

Advances in scientific disciplines that support classical biological control have provided “new tools” that could have important applications for biocontrol programs for some long-established invasive arthropod pests. We suggest that these previously unavailable tools should be used in biological control programs targeting “legacy pests”, even if they have been targets of previously unsuccessful biocontrol projects. Examples of “new tools” include molecular analyses to verify species identities and likely geographic area of origin, climate matching and ecological niche modeling, preservation of natural enemy genetic diversity in quarantine, the use of theory from invasion biology to maximize establishment likelihoods for natural enemies, and improved understanding of the interactions between natural enemy and target pest microbiomes. This review suggests that opportunities exist for revisiting old pest problems and funding research programs using “new tools” for developing biological control programs for “legacy pests” could provide permanent suppression of some seemingly intractable pest problems. As a case study, we use citricola scale, Coccus pseudomagnoliarum, an invasive legacy pest of California citrus, to demonstrate the potential of new tools to support a new classical biological control program targeting this insect.

With the global rise of human‐mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here, we use a biocontrol system to examine the genome‐wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals across laboratory cultures, the native ranges, and the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata × D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.