A benefit-risk analysis for biological control introductions based on the protection of native biodiversity.

The release of biological control agents has been an important means of controlling invasive species for over 150 years. While these releases have led to the sustainable control of over 250 invasive pest and weed species worldwide, a minority have caused environmental harm. A growing recognition of the risks of biological control led to a focus on risk assessment beginning in the 1990s along with a precipitous decline in releases. While this new focus greatly improved the safety of biological control, it came at the cost of lost opportunities to solve environmental problems associated with invasive species. A framework that incorporates benefits and risks of biological control is thus needed to understand the net environmental effects of biological control releases. We introduce such a framework, using native biodiversity as the common currency for both benefits and risks. The model is based on interactions among four categories of organisms: (1) the biological control agent, (2) the invasive species (pest or weed) targeted by the agent, (3) one or more native species that stand to benefit from the control of the target species, and (4) one or more native species that are at risk of being harmed by the released biological control agent. Conservation values of the potentially benefited and harmed native species are incorporated as well, and they are weighted according to three axes: vulnerability to extinction, the ecosystem services provided, and cultural significance. Further, we incorporate the potential for indirect risks to native species, which we consider will result mainly from the ecological process of agent enrichment that may occur if the agent exploits but does not control the target pest or weed. We illustrate the use of this framework by retrospectively analyzing the release of the vedalia beetle, Novius (= Rodolia) cardinalis, to control the cottony cushion scale, Icerya purchasi, in the Galapagos Islands. While the framework is particularly adaptable to biological control releases in natural areas, it can also be used in managed settings, where biological control protects native species through the reduction of pesticide use.

Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israeli citrus orchards.

The citrus rust mite (CRM), Phyllocoptruta oleivora (Acari: Eriophyidae) is a cosmopolitan key pest of citrus, inflicting severe economic damage if not controlled. In Israel, CRM damages all citrus cultivars. International regulation and increasing control failures of CRM led growers to seek sustainable biological control solutions such as acarine biological control agents. Laboratory studies conducted in Israel have indicated that the indigenous predator species Amblyseius swirskii, Iphiseius degenerans, Typhlodromus athiasae and Euseius scutalis (all Acari: Phytoseiidae) can potentially control CRM. Our general objective in the present study was to bridge the gap of knowledge between laboratory studies and the lack of control efficacy of these species in commercial orchards. Predator augmentation in the field showed that although predator populations increased immediately following releases they later decreased and did not affect CRM populations. When A. swirskii augmentation was combined with a series of maize pollen applications, A. swirskii populations were enhanced substantially and continuously but again CRM populations were not affected. Growth chamber studies with CRM-infested seedlings, with or without a maize pollen supplement, indicated that pollen provisioning led to population increase of E. scutalis and A. swirskii but only E. scutalis significantly lowered CRM populations. Control with E. scutalis was confirmed in the field on CRM infested seedlings with pollen provisioned by adjacent flowering Rhodes grass. While experiments in mature citrus orchard showed that pollen supplement usually increased predator populations they also indicated that other factors such as intraguild interactions and pesticide treatments should be taken into account when devising CRM biological control programs.

Negative Effects of Phthorimaea absoluta-Resistant Tomato Genotypes on the Zoophytophagous Biocontrol Agent, Orius laevigatus (Fieber) (Hemiptera: Anthocoridae).

Complex interactions between host plant resistance (HPR) and biological control agents, particularly omnivorous predators, can shape the outcome of an integrated pest management (IPM) program. However, such interactions are seldom explored during plant breeding programs. Therefore, in the present study, we compared the performance of the omnivorous biological control agent Orius laevigatus on six tomato genotypes with different levels of resistance to the tomato leaf miner Phthorimaea absoluta. We found that the O. laevigatus fitness components (i.e., egg deposition, egg hatching rate, and duration of egg, early nymphal, late nymphal stages, and their survival) were inferior on the wild resistant genotypes (LA 716 and LA 1777) in comparison to the resistant domesticated genotype EC 620343 and the susceptible genotypes (EC 705464 and EC 519819). It appears that the adverse effects of tomato genotypes on O. laevigatus are determined mainly by glandular and non-glandular trichome densities on the leaves. Comparison of O. laevigatus response to the tested tomato cultivars to that of P. absoluta revealed significant positive correlations in duration of the egg stages, development time of early and late larval stages, and overall immature mortality in both species. It appears, therefore, that defensive plant traits operate in a similar way on the pest and its predator in the system. Overall, the present study of the tomato-P. absoluta-O. laevigatus system provides experimental evidence for the need to optimize pest management by employing intermediate levels of crop resistance together with biological control agents.

Life-table analyses for the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae): effects of plant genotype.

BACKGROUND: Host plant resistance plays an important role in integrated pest management programs. Crop resistance assessments commonly focus on only a single dependent variable, such as larval survival/plant damage, which limits the ability to appreciate the impact of host plants on pest populations in the full sense. Therefore, we performed life-table analyses for tomato leaf miner Tuta absoluta, on 19 Solanum lycopersicum genotypes and a wild Solanum habrochaites accession. These analyses assess the ability of the pest to attain a high population density on different tomato genotypes. Based on the resulting ranking of tomato resistance at the vegetative stage (45-day-old plants), we tested the resistance of six selected genotypes at the reproductive stage (4-month-old plants). RESULTS: T. absoluta performance was significantly inferior on vegetative-stage S. habrochaites plants (LA 1777); time taken for the first instars to mine the leaves (5 ± 0.14 days), development time of early- and late-stage larvae (8.8 ± 0.2 and 4.2 ± 0.2 days, respectively), pupal period (11.2 ± 0.58 days), and total developmental time (29.4 ± 0.83 days) were significantly longer, fecundity was significantly lower (18.66 ± 7.24 days), and the highest total mortality (63.33%) also recorded compared with other genotypes, resulting in the lowest net reproductive rate (R0 ) (11.20 ± 2.51). For the six selected genotypes, the ranking of plant resistance did not change between plants at the vegetative and reproductive stages. CONCLUSION: This study suggested that of 20 screened tomato genotypes, LA 1777 and EC-620343 are the least suitable hosts for T. absoluta to establish fast-growing populations, and thus can be employed in integrated T. absoluta management. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Complex Effects of a Land-Use Gradient on Pollinators and Natural Enemies: Natural Habitats Mitigate the Effects of Aphid Infestation on Pollination Services.

Pollinators and natural enemies are essential ecosystem service providers influenced by land-use and by interactions between them. However, the understanding of the combined impacts of these factors on pollinator and natural enemy activities and their ultimate effects on plant productivity remains limited. We investigated the effects of local and landscape vegetation characteristics and the presence of herbivorous pests on pollination and biological control services and their combined influence on phytometer seed set. The study was conducted in a Mediterranean agro-ecosystem, encompassing ten shrubland plots spanning a land-use gradient. Within each plot, we placed caged and uncaged potted phytometer plants that were either aphid-infested or aphid-free. We quantified insect flower visitation, aphid predation and parasitism rates, and fruit and seed set. We found scale-dependent responses of pollinators and natural enemies to land-use characteristics. Flower species richness had a positive impact on aphid parasitism rates but a negative effect on pollinator activity. Notably, we found a more pronounced positive effect of natural areas on pollinator activity in aphid-infested compared to aphid-free plants, indicating a potentially critical role of natural habitats in mitigating the adverse effects of aphid infestation on pollination services. These results highlight the complex and interactive effects of land-use on pollinators and natural enemies, with significant implications for plant productivity.

Analysis of apocarotenoid volatiles from lettuce (Lactuca sativa) induced by insect herbivores and characterization of carotenoid cleavage dioxygenase gene.

Plant apocarotenoids have been shown to have a diverse biological role in herbivore-plant interactions. Despite their importance, little is known about herbivores' effect on apocarotenoid emissions in Lactuca sativa. In this study, we examined changes in apocarotenoid emissions in lettuce leaves after infestation by two insects, viz., Spodoptera littoralis larvae and Myzus persicae aphids. We found that ß-ionone and ß-cyclocitral showed higher concentrations than the other apocarotenoids, with a significant increase as per the intensity of infestation of both herbivore species. Furthermore, we performed functional characterization of Lactuca sativa carotenoid cleavage dioxygenase 1 (LsCCD1) genes. Three LsCCD1 genes were overexpressed in E. coli strains, and recombinant proteins were assayed for cleavage activity on an array of carotenoid substrates. The LsCCD1 protein cleaved ß-carotene at the 9,10 (9',10') positions producing ß-ionone. The transcript analysis of LsCCD1 genes revealed differential expression patterns under varying levels of herbivores' infestation, but the results were inconsistent with the pattern of ß-ionone concentrations. Our results suggest that LsCCD1 is involved in the production of ß-ionone, but other regulatory factors might be involved in its induction in response to herbivory. These results provide new insights into apocarotenoid production in response to insect herbivory in lettuce. Supplementary Information: The online version contains supplementary material available at 10.1007/s13205-023-03511-4.

Identification of Orius (Heteroptera: Anthocoridae) females based on egg operculum structure.

Naturally occurring predators of the genus Orius (Heteroptera: Anthocoridae) often suppress agricultural pests in insecticide-free environments. Knowledge of Orius species composition in the field is important because species vary in their biology, prey preference, and ability to suppress pest populations. However, field-collected Orius bugs are often female biased and the identification of Orius females may be unreliable and time consuming. Identification of Orius species based on egg structure may allow easy and nondestructive identification of females, by inspecting the eggs they deposit, and identification of species that reproduce in the field. The aim of the current study was to illustrate how several Mediterranean Orius species could be identified using egg opercula. For this purpose, the structure of the operculum was described for eggs deposited by field-collected females, based on scanning electron microscope images. Then, adult males that developed from these eggs were identified to species by genitalia examination. A detailed description of diagnostic features of the operculum is given for each of four Orius species: O. albidipennis (Reuter), O. niger Wolff, O. laevigatus (Fieber), and O. horvathi (Reuter). Characterizing the structure of egg opercula of additional Orius species would facilitate ecological and biological control research in other parts of the world.

Rickettsia association with two Macrolophus (Heteroptera: Miridae) species: A comparative study of phylogenies and within-host localization patterns.

Many arthropods host bacterial symbionts, some of which are known to influence host nutrition and diet breadth. Omnivorous bugs of the genus Macrolophus (Heteroptera: Miridae) are mainly predatory, but may also feed on plants. The species M. pygmaeus and M. melanotoma (=M. caliginosus) are key natural enemies of various economically important agricultural pests, and are known to harbor two Rickettsia species, R. bellii and R. limoniae. To test for possible involvement of symbiotic bacteria in the nutritional ecology of these biocontrol agents, the abundance, phylogeny, and distribution patterns of the two Rickettsia species in M. pygmaeus and M. melanotoma were studied. Both of the Rickettsia species were found in 100 and 84% of all tested individuals of M. pygmaeus and M. melanotoma, respectively. Phylogenetic analysis showed that a co-evolutionary process between Macrolophus species and their Rickettsia is infrequent. Localization of R. bellii and R. limoniae has been detected in both female and male of M. pygmaeus and M. melanotoma. FISH analysis of female gonads revealed the presence of both Rickettsia species in the germarium of both bug species. Each of the two Rickettsia species displayed a unique distribution pattern along the digestive system of the bugs, mostly occupying separate epithelial cells, unknown caeca-like organs, the Malpighian tubules and the salivary glands. This pattern differed between the two Macrolophus species: in M. pygmaeus, R. limoniae was distributed more broadly along the host digestive system and R. bellii was located primarily in the foregut and midgut. In contrast, in M. melanotoma, R. bellii was more broadly distributed along the digestive system than the clustered R. limoniae. Taken together, these results suggest that Rickettsia may have a role in the nutritional ecology of their plant-and prey-consuming hosts.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes.

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Incorporation of intraguild predation into a pest management decision-making tool: the case of thrips and two pollen-feeding predators in strawberry.

Action thresholds are traditionally based on the density of pests and the economic damage they cause to crops. Pest damage assessments are usually made in a "sterile" environment, devoid of extenuating factors such as predators, parasitoids, and alternative food sources. Recently, the effects of a predator or parasitoid species have been considered. However, interactions between natural enemy species (intraguild predation and interference), which are common in agricultural fields, have not been incorporated yet into decision-making tools. We conducted a series of leaf disc and potted plant trials to evaluate the effects of two predator species, the anthocorid Orius laevigatus (Fieber) and the phytoseiid Neoseiulus cucumeris (Oudemans) on the density of and fruit damage inflicted by western flower thrips, Frankliniella occidentalis (Pergande). We then used the obtained results to develop a pest management decision-making tool for the control of western flower thrips. Because strawberries (Fragaria x ananassa Duchesne) flower in cycles, pollen, a food source for both predators and the pest, is periodically available in the system and has also been incorporated in our decision-making tool. The developed new management tool would allow the relaxation of the economic threshold (ET) for western flower thrips in strawberry flowers. The presence of an average of a single O. laevigatus per flower for example, may allow that relaxation of the ET by 40% (from 10 to 14 western flower thrips per flower) when pollen is available during the winter. Because field monitoring shows that O. laevigatus populations in Israeli strawberry often reach mean densities of three to four per flower, the new approach promises to drastically reduce the employment of toxic insecticides.

Cellular Localization of Two Rickettsia Symbionts in the Digestive System and within the Ovaries of the Mirid Bug, Macrolophous pygmaeus.

Bacterial symbionts in arthropods are common, vary in their effects, and can dramatically influence the outcome of biological control efforts. Macrolophus pygmaeus (Heteroptera: Miridae), a key component of biological control programs, is mainly predaceous but may also display phytophagy. M. pygmaeus hosts symbiotic Wolbachia, which induce cytoplasmic incompatibility, and two Rickettsia species, R. bellii and R. limoniae, which are found in all individuals tested. To test possible involvement of the two Rickettsia species in the feeding habits of M. pygmaeus, we first showed that the microbiome of the insect is dominated by these three symbionts, and later described the distribution pattern of the two Rickettsia species in its digestive system. Although both Rickettsia species were located in certain gut bacteriocyes, in caeca and in Malpighian tubules of both sexes, each species has a unique cellular occupancy pattern and specific distribution along digestive system compartments. Infrequently, both species were found in a cell. In females, both Rickettsia species were detected in the germarium, the apical end of the ovarioles within the ovaries, but not in oocytes. Although the cause for these Rickettsia distribution patterns is yet unknown, it is likely linked to host nutrition while feeding on prey or plants.

Parasitized aphids are inferior prey for a coccinellid predator: implications for intraguild predation.

Discussions of intraguild predation (IGP) have assumed that the nutritional quality of intraguild (IG) prey is similar to that of any other prey available to the IG predator. It has been suggested therefore that generalist predators do not distinguish between healthy and parasitized aphids and thus function as facultative predators of parasitoids. More recent studies have shown that predators may selectively ingest prey of various nutritional qualities and that predators may have higher body nitrogen composition than herbivores. If so, predators may preferentially feed on other predators (i.e., IG prey) to increase their nitrogen intake. We used a system composed of larvae of the coccinellid Coccinella undecimpunctata (IG predator), the parasitoid Aphidius colemani (IG prey), and their shared food source, the green peach aphid Myzus persicae, to test whether (1) the predator preferentially feeds on parasitized over healthy prey, (2) predatory behavior on parasitized aphids changes with time elapsed after parasitism, and (3) parasitized and healthy aphids differ in their suitability for predator development. Results indicate that, given a choice, C. undecimpunctata larvae show no preference for either parasitized or healthy prey items, regardless of parasitoid age. Feeding time, however, increased with parasitoid age, leading to a reduction in the number of prey consumed per unit time. Mummified prey were protected from predation by C. undecimpunctata larvae but the larvae were able to feed and complete development on mummies with a broken cuticle. These predators, however, had an extended developmental time and lower pupal and adult weights in comparison to larvae fed healthy aphids. That parasitized aphids are inferior prey for C. undecimpunctata larvae should act to reduce intensity of IGP in the field and the negative impact IGP has on herbivore suppression.

Estimating the effect of plant-provided food supplements on pest consumption by omnivorous predators: lessons from two coccinellid beetles.

BACKGROUND: Plant-provided food supplements can influence biological pest control by omnivorous predators in two counteracting ways: they can (i) enhance predator populations, but (ii) reduce pest consumption by individual predators. Yet the majority of studies address only one of these aspects. Here, we first tested the influence of canola (Brassica napus L.) pollen supplements on the life history of two ladybeetle species: Hoppodamia variegata (Goeze) and Coccinella septempunctata (L.). We then developed a theoretical model to simulate total pest consumption in the presence and absence of pollen supplements. RESULTS: Supplementing a prey diet with canola pollen increased H. variegata larval survival from 50 to 82%, and C. septempunctata female oviposition by 1.6-fold. Model simulations revealed a greater benefit of pollen supplements when relying on C. septempunctata for pest suppression than on H. variegata. CONCLUSION: For these two predators, the tested pollen serves as an essential supplement to a diet of prey. However, the benefit of a mixed prey-pollen diet was not always sufficient to overcome individual decrease in pest consumption. Taken together, our study highlights the importance of addressing both positive and negative roles of plant-provided food supplements in considering the outcome for biological control efforts that rely on omnivorous predators. © 2016 Society of Chemical Industry.

Prey and Pollen Food Choice Depends on Previous Diet in an Omnivorous Predatory Mite.

The time allocated by omnivorous predators to consuming prey versus plant-provided foods (e.g., pollen) directly influences their efficacy as biocontrol agents of agricultural pests. Nonetheless, diet shifting between these two very different food sources remains poorly understood. We hypothesized that previous diet composition influences subsequent choice of prey and plant food types. We tested this hypothesis by observing the foraging choices of Amblyseius swirskii (Athias-Henriot) mites (Mesostigmata: Phytoseiidae), which were first maintained on either prey (broad mites) or corn pollen, and then offered familiar and unfamiliar foods. A. swirskii exhibited strong fidelity to familiar food, whether prey or pollen, suggesting there are physiological or behavioral costs involved in shifting between such different foods. Results illustrate the importance of previous diet for subsequent pest consumption by omnivorous natural enemies.

Intraguild interactions among specialised pollen feeders and generalist phytoseiids and their effect on citrus rust mite suppression.

BACKGROUND: Antagonistic interactions among predators with shared prey are thought to hamper their ability to suppress herbivores. Our aim was to quantify intraguild interactions in omnivorous predatory mite assemblages in the presence of pollen, and assess their effect on pest populations. We focused on the following naturally occurring phytoseiid species in Israeli citrus orchards and their ability to suppress a key pest, the citrus rust mite (CRM) Phyllocoptruta oleivora (Eriophyidae): the generalists Amblyseius swirskii and Typhlodromus athiasae and the specialised pollen feeders Iphiseius degenerans, Euseius scutalis, E. stipulatus and E. victoriensis. Evaluations were performed on two spatial scales, tree seedlings and leaf discs. RESULTS: On seedlings, experiments were conducted to quantify the interactions between predators in the presence of pollen and its effects on CRM suppression. On leaf discs, intraguild interactions were studied between pairs of phytoseiid species in the presence of pollen without CRM. On seedlings, the specialised pollen predators were more effective at suppressing CRM populations than the generalist predators. CONCLUSION: In most cases, the more aggressive intraguild predator was the specialised pollen feeder. Similarly, leaf-disc experiments suggest that in these interactions the specialised pollen feeders tend to be the intraguild predators more often than the intraguild prey.

Feeding and ovipositing on plants by an omnivorous insect predator.

Omnivory (i.e., feeding at more than one trophic level) is common in many ecological communities. To date, most studies of omnivory have focused on systems that include omnivores that feed on several prey items, primarily in aquatic systems. Yet, many terrestrial insect predators feed not only on prey but also on plants. The difference between systems with plant-feeding omnivores and those with exclusively prey-feeding omnivores calls for special attention. The first step towards understanding the interactions between plant-feeding omnivores and their prey is to determine how omnivores respond to variations in plant properties. In this study, I investigated two major aspects of the interactions between the plant-feeding predatory bug Orius insidiosus and four host plants of its prey; the behavioral aspect, in which plants are selected for oviposition and the physiological aspect, in which plants differ in their suitability for the insect's growth, survival, and reproduction. No prey was offered to the omnivore during any of the experiments, but older nymphs and adults were fed prey eggs prior to their use in the experiments. Data show that O. insidiosus females almost completely rejected corn leaves for oviposition; nymph and adult survival was highest on bean; and female fecundity was higher on bean than tomato, pepper or corn foliage. the significance of the apparent ability of O. insidiosus to discriminate among plants and the observed correlation between oviposition preference and offspring performance in bean and in corn is discussed.

Effects of Global Warming on Predatory Bugs Supported by Data Across Geographic and Seasonal Climatic Gradients.

Global warming may affect species abundance and distribution, as well as temperature-dependent morphometric traits. In this study, we first used historical data to document changes in Orius (Heteroptera: Anthocoridae) species assemblage and individual morphometric traits over the past seven decades in Israel. We then tested whether these changes could have been temperature driven by searching for similar patterns across seasonal and geographic climatic gradients in a present survey. The historical records indicated a shift in the relative abundance of dominant Orius species; the relative abundance of O. albidipennis, a desert-adapted species, increased while that of O. laevigatus decreased in recent decades by 6 and 10-15 folds, respectively. These shifts coincided with an overall increase of up to 2.1°C in mean daily temperatures over the last 25 years in Israel. Similar trends were found in contemporary data across two other climatic gradients, seasonal and geographic; O. albidipennis dominated Orius assemblages under warm conditions. Finally, specimens collected in the present survey were significantly smaller than those from the 1980's, corresponding to significantly smaller individuals collected now during warmer than colder seasons. Taken together, results provide strong support to the hypothesis that temperature is the most likely driver of the observed shifts in species composition and body sizes because (1) historical changes in both species assemblage and body size were associated with rising temperatures in the study region over the last few decades; and (2) similar changes were observed as a result of contemporary drivers that are associated with temperature.

Omnivory in terrestrial arthropods: mixing plant and prey diets.

Many terrestrial communities include omnivorous arthropods that feed on both prey and plant resources. In this review we first discuss some unique morphological, physiological, and behavioral traits that enable omnivores to exploit such dissimilar foods, and we explore possible evolutionary pathways to omnivory. We then examine possible benefits and costs of omnivory, describe the relationships between omnivory and other high-order complex trophic interactions, and consider the stability level of communities with closed-loop omnivory. Finally, we explore some of the implications of omnivory for crop damage and for biological, chemical, and cultural control practices. We conclude that the growing realization of the ubiquity of omnivory in nature may require a change in our view of the structure and function of ecological systems.