Generalist Natural Enemies Research Articles

Can genomic signatures guide the selection of host-specific agents for weed biological control?

Biological control of weeds involves deliberate introduction of host-specific natural enemies into invaded range to reduce the negative impacts of invasive species. Assessing the specificity is a crucial step, as introduction of generalist natural enemies into a new territory may pose risks to the recipient communities. A mechanistic understanding of host use can provide valuable insights for the selection of specialist natural enemies, bolster confidence in non-target risk assessment and potentially accelerate the host specificity testing process in biological control. We conducted a comprehensive analysis of studies on the genomics of host specialization with a view to examine if genomic signatures can help predict host specificity in insects. Focusing on phytophagous Lepidoptera, Coleoptera and Diptera, we compared chemosensory receptors and enzymes between "specialist" (insects with narrow host range) and "generalist" (insects with wide host range) insects. The availability of genomic data for biological control agents (natural enemies of weeds) is limited thus our analyses utilized data from pest insects and model organisms for which genomic data are available. Our findings revealed that specialists generally exhibit a lower number of chemosensory receptors and enzymes compared with their generalist counterparts. This pattern was more prominent in Coleoptera and Diptera relative to Lepidoptera. This information can be used to reject agents with large gene repertoires to potentially accelerate the risk assessment process. Similarly, confirming smaller gene repertoires in specialists could further strengthen the risk evaluation. Despite the distinctive signatures between specialists and generalists, challenges such as finite genomic data for biological control agents, ad hoc comparisons, and fewer comparative studies among congeners limit our ability to use genomic signatures to predict host specificity. A few studies have empirically compared phylogenetically closely related species, enhancing the resolution and the predictive power of genomics signatures thus suggesting the need for more targeted studies comparing congeneric specialists and generalists.

Soil fertility as a mediator of interactions between an introduced specialist beetle and a native generalist nematode on an exotic invasive plant and its native congener

Abstract Invasive plants are often attacked by both introduced specialist and native generalist natural enemies in new ranges. Soil fertility can potentially alter the interactions of these natural enemies with native versus invasive plants in ways that have largely unexplored implications for biological invasions and biological control. A common garden experiment was conducted to compare the performance of an introduced specialist flea beetle, Agasicles hygrophila, and/or a native generalist nematode, Meloidogyne incognita, on invasive alligator weed, Alternanthera philoxeroides, and its native congener sessile joyweed, Alternanthera sessilis, under different levels of soil nitrogen (N) and phosphorus (P). At a relatively low or moderate N and P levels, the flea beetle and the nematodes were not significantly affected by each other. Under these conditions, alligator weed responded plastically by producing more branches and biomass, as well as longer stolons, in response to attack by the flea beetle and/or the nematode, compared to sessile joyweed responses to similar levels of damage. However, under a relatively high N and P levels, nematode infestations significantly reduced flea beetle damage on alligator weed, resulting in significantly greater above‐ and below‐ground biomass and longer stolons than plants without herbivory. In contrast, beetle herbivory significantly increased the level of nematode infestations on sessile joyweed, resulting in significantly fewer fine and coarse roots, and lower above‐ and below‐ground biomass compared to plants without herbivory. Synthesis and applications. Our findings illustrate the importance of soil fertility in mediating interactions between specialist biocontrol agents and native generalists on native versus invasive plants. High phenotypic plasticity seems to be an important attribute that contributes to the success of invasive plants like alligator weed in relatively nutrient‐poor environments. However, nutrient‐rich environments could potentially confer greater growth benefits on invasive plants than on native ones by changing herbivore–herbivore interactions on plants differently. There is a great need to fully investigate the direct and indirect interactions between biocontrol agents and generalists across food webs following classical biocontrol releases. Nutrient measurements of both soil and water bodies should also be incorporated into all stages of biocontrol programmes.

Habitat Diversity Increases Chrysoperla carnea s.l. (Stephens, 1836) (Neuroptera, Chrysopidae) Abundance in Olive Landscapes

Chrysoperla carnea s.l., a vital predator in olive groves, plays a key role in reducing the reliance on pesticides. Despite its efficacy, habitat diversification at the landscape level can compromise its effectiveness as a generalist natural enemy, diverting its attention from olive pests to other resources. To unravel its habitat preferences and maximize biocontrol services, a comprehensive study was conducted, collecting specimens monthly across diverse habitats in a Portuguese olive grove landscape. These habitats included shrublands, “montado,” grasslands, eucalyptus and pine forests, vineyards, and olive groves. The findings revealed C. carnea s.l. displayed a widespread presence in all habitats, with peak abundance initially observed in olive groves, coinciding with the presence of its preferred prey, Prays oleae. However, the peak abundance of this species varies among habitats, with the highest numbers initially observed in olive groves, gradually decreasing throughout the summer and reaching the lowest levels in vineyards. Significantly, habitat diversification at the landscape level contributes to an increased abundance of C. carnea s.l. in olive groves. This suggests that diversifying available resources aids in sustaining natural enemy populations in proximity to the targeted crop, thereby enhancing their efficacy in pest control. Consequently, we advocate for stakeholders in olive cultivation to promote landscape-scale habitat diversity by preserving, restoring, or fostering alternative habitats surrounding olive groves.

Ecology and management of the crapemyrtle aphid (Hemiptera: Aphididae) on crapemyrtle (Myrtales: Lythraceae) in the southern United States

Abstract Crapemyrtle aphid [Sarucallis kahawaluokalani (Kirkaldy 1907)] (CMA) is an introduced pest of crapemyrtle (Lagerstroemia spp. L.), which is among the most common ornamental tree genera in the southern United States. Native to Southeast Asia, CMA has become established on 5 other continents. CMAs produce honeydew as they feed which supports sooty mold growth and can result in leaf defoliation on infested trees. CMAs tend to be most abundant in crapemyrtles planted in locations with extensive surrounding impervious surface cover. A large community of generalist natural enemies are found in close association with CMA, which suggests that CMAs may help conserve natural enemy communities in urban areas. Due to the long-lasting blooms produced by crapemyrtle, and the attractiveness of these blooms to pollinators, insecticides should be used as a last resort to manage CMA infestations. While CMA is considered a specialist pest of crapemyrtle, it has been recorded on 3 species outside of the genus Lagerstroemia. The wide distribution of CMA, closely overlapping that of crapemyrtle, suggests that CMA can likely be found wherever crapemyrtles are commonly planted.

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UNDERSTANDING THE SEARCHING BEHAVIOUR OF PREDATOR AND PARASITOID INSECTS: A REVIEW

The aim of this review is to understand whether the searching behaviour of natural enemies (parasitoids and predators) is affected by complex odour mixtures and if there are differences between specialist and generalist natural enemies. To accomplish this objective, a literature review of several research papers related to the topic was done. Natural enemies of herbivores mainly use herbivore induced plant volatiles (HIPVs) to find their prey or host. However, the chemical information conveyed through HIPVs toward natural enemies might be unreliable or sometimes undetectable for them (odour masking), thereby influencing their searching behaviour. Many factors influence the reliability and detectability of HIPVs such as: plant diversity, intensity of the herbivore attack, if one or more herbivore species attack the plant at the same time or sequentially, and environmental conditions like light intensity, fertilization levels, soil moisture, and high concentrations of ozone, hydroxyl, and nitrate radicals. Nevertheless, in order to overcome reliability and detectability problems of HIPVs, natural enemies have the ability to learn by association and use these HIPVs to find their prey or host. Further field experiments supported by laboratory assessments should be carried out to understand how the searching behaviour of natural enemies is affected in a multitrophic level context, where known biodiversity (above and below ground) and environmental conditions have the possibility to interact.

Alternative food sources for Amblydromella caudiglans (Phytoseiidae) and effects on predation.

The addition of supplemental food sources for natural enemies is a growing component of conservation and augmentative biological control. Supplemental foods can be used to retain natural enemies when prey are scarce and to promote survival, fecundity, longevity, and development of natural enemy populations, especially generalist natural enemies. Amblydromella caudiglans (Schuster) (Acari: Phytoseiidae) is one of the most abundant predatory mites found in commercial apple orchards in Washington, USA, and contributes to spider mite control. However, because its widespread presence in commercial apple orchards was only recently discovered, how supplementary food sources affect its performance is unknown. In laboratory studies, we evaluated the performance (fecundity, retention, prey consumption) of the generalist phytoseiid A. caudiglans on commercially available supplemental food sources, including factitious prey (Ephestia eggs and Artemia brine shrimp cysts), and pollens of apple, pear, and cattail. We determined that A. caudiglans will not consume Ephestia eggs and performs best on cattail and pear pollens. Combinations of food sources did not enhance the performance of this predator compared to the best performing single-sources. The presence of alternative food sources did not decrease A. caudiglans predation of twospotted spider mite nymphs, except for Artemia brine shrimp cysts, which had a substantial handling time. These results lay the groundwork for identifying a way to promote and retain this natural enemy in tree fruit cropping systems through the use of food resource applications or floral plantings.

Native generalist natural enemies and an introduced specialist parasitoid together control an invasive forest insect.

Specialized natural enemies have long been used to implement the biological control of invasive insects. Although research tracking populations following biological control introductions has traditionally focused on the impact of the introduced agent, recent studies and reviews have reflected an appreciation of the complex interactions of the introduced specialist agents with native generalist natural enemies. These interactions can be neutral, antagonistic, or complementary. Here we studied the invasive defoliator winter moth (Operophtera brumata) in the Northeast USA to investigate the role of native, generalist pupal predators along with the introduced, host-specific parasitoid Cyzenis albicans. Prior research in Canada has shown that predation of winter moth pupae from native generalists increased after C. albicans was established as a biological control agent. To explain this phenomenon, the following hypotheses were suggested: (H1 ) parasitoids suppress the winter moth population to a density that can be maintained by generalist predators, (H2 ) unparasitized pupae are preferred by predators and therefore experience higher mortality rates, or (H3 ) C. albicans sustains higher predator populations throughout the year more effectively than winter moth alone. We tested these hypotheses by deploying winter moth pupae over 6 years spanning 2005 to 2017 and by modeling pupal predation rates as a function of winter moth density and C. albicans establishment. We also compared predation rates of unparasitized and parasitized pupae and considered additional mortality by a native pupal parasitoid. We found support for the first hypothesis; we detected both temporal and spatial density dependence, but only in the latter years of the study when winter moth densities were low. We found no evidence for the latter two hypotheses. Our findings suggest that pupal predators have a regulatory effect on winter moth populations only after populations have been reduced, presumably by the introduction of the host-specific parasitoid C. albicans.

Effect of Conservation Agriculture on Aphid Biocontrol by Generalist (Carabid Beetle) and Specialist (Parasitoids Wasp) Natural Enemy Communities in Winter Wheat

Adoption of practices that reduce the risk of pest outbreaks is one of the pillars of agroecology and is largely based on biological control. Multiple infield and landscape parameters affect biocontrol, but the effects of conservation soil management on biological control have been poorly investigated over crop season. By comparing winter wheat fields within the same landscape but with different soil management, the direct and indirect effects of soil management (conservation and conventional systems) on natural enemies’ communities and their biological control on aphids was studied from the tillering stage to the harvest. In addition to aphid infestation, two families of the main natural enemies’ guilds were monitored, as well as their associated services: aphid parasitoid, a specialist and flying natural enemy, with parasitism service, and carabid beetles, a generalist and ground-dwelling predator, with aphidophagy service. Soil conservation system hosted more abundant and diverse carabid beetles’ assemblages, and received higher aphidophagy service in June than conventional system. However, neither parasitoid abundance, nor parasitism rates, were affected by soil management. Aphid infestation and its associated damage did not depend on soil management either. Our results suggest that ground-dwelling natural enemies are more impacted by soil management than foliage-dwelling natural enemies, which is partly reflected in aphid biocontrol. In agricultural systems with reduced soil perturbation, direct mortality on ground-dwelling communities due to tillage may be lower than in a conventional system, but habitat heterogeneity is also greater, increasing the number of ecological niches for natural enemies. Both factors are supposed to favor an early presence of natural enemies and a tendency toward a precocious aphidophagy service is indeed observed in conservation system.

A Review of Franklinothrips vespiformis (Thysanoptera: Aeolothripidae): Life History, Distribution, and Prospects as a Biological Control Agent.

Simple SummaryPredatory species are a small but significant part of the Thysanoptera, which is often overlooked. Franklinothrips are found throughout the tropics and are regarded as major natural enemies of thrips and other small arthropod prey. In this review, we summarized the geographical background, morphology, and prey associations, with an emphasis on Franklinothrips vespiformis, the most widely distributed predatory thrips species. This literature review could serve as a foundation for future research into Franklinothrips as biocontrol agents for economically important insect and mite pests in China.Predatory species comprise a small but important and often overlooked component of the Thysanoptera. A case in point, the ant-mimicking Franklinothrips are widely distributed in the tropics and are considered important generalist natural enemies for thrips and some other small arthropod prey. Franklinothrips present an addition to biocontrol applications, i.e., greenhouse or commercial application for certain target pests and situations. Current knowledge, including distribution, biological features, life history pa rameters, prey specificity, host plant associations and lass production is yet insufficient to decide to what extent Franklinothrips could contribute for biological control programs. In this review, we summarized the geographical background, morphology, and prey associations, with a focus on F. vespiformis, the most widely distributed species of predatory thrips. This literature review serves as the basis for future research into the use of Franklinothrips as biocontrol agents for economically significant insect and mite pests in China and elsewhere.

Survey and population dynamics of cereal aphids and their common natural enemies inhabiting wheat crop in Hail region, Saudi Arabia

AbstractCereal aphids are known as serious pests that cause considerable yield losses of wheat production. In this study, cereal aphids and their common natural enemies inhabiting the commercial wheat crop were investigated between February and April 2013 as a preliminary study in the Hail region, northern Saudi Arabia. Results showed that wheat crops were infested by four aphid species including the Russian wheat aphid Diuraphis noxia Kurdjumov, the English grain aphid Sitobion avenae Fabricius, the bird cherry‐oat aphid Rhopalosiphum padi L. and the greenbug aphid Schizaphis graminum Rondani (Homoptera: Aphididae). The Russian wheat aphid D. noxia, however, was the most abundant species compared to other aphid species, totaling 343 individuals which represented 39.80% of all cereal aphids. The results showed a diverse community of specialist natural enemies that were associated aphids including parasitoid wasps as a complex and one Braconid species Aphidius matricariae Haliday (Hymenoptera: Braconidae), three coccinellid species (Adonia variegate Goeze, Coccinella quinquepunctata L. and Coccinella septimpunctata L.) (Coleoptera: Coccinellidae), one species of lacewing Chrysopa sp. (adults &amp; larvae) (Neuroptera: Chrysopidae) and one species of hoverfly Eristalinus aeneus Scop. (adults and larvae) (Diptera: Syrphidae). This study, also, recorded a high abundance of polyphagous predators that included two species of ground beetles involving the black beetle Calosoma olivieri Dejean and Calosoma imbricatum Klug (Coleoptera: Carabidae), and spiders (Araneae) as generalist natural enemies of cereal aphids. In this article, population dynamics of captured cereal aphids and their common natural enemies, and their correlations will be described and discussed.

IMPACT OF NATURAL ENEMIES ON LARVAE OF THAUMETOPOEA BONJEANI (LEPIDOPTERA NOTODONTIDAE) IN ASSOCIATION WITH THAUMETOPOEA PITYOCAMPA IN NORTHERN ALGERIA

The cedar processionary moth, Thaumetopoea bonjeani (Lepidoptera: Notodontidae), is a serious pest of the Atlas cedar Cedrus atlantica in north-western Africa and it is involved in the decline of this endangered tree species. Natural enemies of the cedar processionary moth are poorly known, especially for parasitoids, predators and pathogens of the larval-pupal life stages. Mature larvae were collected and examined in 2014 and 2015 in natural stands of Atlas cedar in the Djurdjura (northern Algeria), in occurrence with pine processionary moth Thaumetopoea pityocampa. The overall mortality rate of larvae of Thaumetopoea bonjeani ranged from 26.4% to 31.1%, with generalist predators and parasitoids being more effective than pathogens. Four primary parasitoid species were recorded, of which four tachinid flies and one braconid wasp, as well as four predatory beetles and one fungus. The most important species were the carabid Calosoma sycophanta and the tachinid Compsilura concinnata. The cooccurrence of T. bonjeani and T. pityocampa may offer to generalist natural enemies an extended period of availa- bility of similar preys, as the two processionary moths have different life cycles. The sharing of natural enemies between the two species of Thaumetopoea can mitigate the outbreaks of both species.

Natural enemies have inconsistent impacts on the coexistence of competing species.

The role of natural enemies in promoting coexistence of competing species has generated substantial debate. Modern coexistence theory provides a detailed framework to investigate this topic, but there have been remarkably few empirical applications to the impact of natural enemies. We tested experimentally the capacity for a generalist enemy to promote coexistence of competing insect species, and the extent to which any impact can be predicted by trade-offs between reproductive rate and susceptibility to natural enemies. We used experimental mesocosms to conduct a fully factorial pairwise competition experiment for six rainforest Drosophila species, with and without a generalist pupal parasitoid. We then parameterised models of competition and examined the coexistence of each pair of Drosophila species within the framework of modern coexistence theory. We found idiosyncratic impacts of parasitism on pairwise coexistence, mediated through changes in fitness differences, not niche differences. There was no evidence of an overall reproductive rate-susceptibility trade-off. Pairwise reproductive rate-susceptibility relationships were not useful shortcuts for predicting the impact of parasitism on coexistence. Our results exemplify the value of modern coexistence theory in multi-trophic contexts and the importance of contextualising the impact of generalist natural enemies to determine their impact. In the set of species investigated, competition was affected by the higher trophic level, but the overall impact on coexistence cannot be easily predicted just from knowledge of relative susceptibility. Methodologically, our Bayesian approach highlights issues with the separability of model parameters within modern coexistence theory and shows how using the full posterior parameter distribution improves inferences. This method should be widely applicable for understanding species coexistence in a range of systems.

Foraging aggressiveness determines trophic niche in a generalist biological control species

AbstractThere is a growing evidence that consistent interindividual differences in behavior, that is, behavioral types, can play an important role in key ecological processes such as predator–prey interactions, which in turn can have direct implications on biological control. Behavioral types of generalist predators may affect these interactions through individual differences in predators’ prey preferences and the breadth of predators’ trophic niches. This study examined how the multivariate nature of behavior, namely foraging aggressiveness, activity level, and risk-taking behavior, determines prey selection and trophic niche of the generalist agrobiont spider Philodromus cespitum. In laboratory experiments, we determined the repeatability of these behaviors and the preference between crickets, moths, fruit flies, and collembolans. We found that all three behaviors were moderately to strongly repeatable but there were no correlations between them, thus they did not form a behavioral syndrome. Only foraging aggressiveness influenced the prey selection of philodromid spiders and the more aggressive individuals had wider trophic niches because they incorporated prey that were more difficult to capture in their diet. In addition, more aggressive individuals killed a greater quantity of particular prey types while other prey types were killed at a similar rate by both aggressive and nonaggressive individuals. The differences in philodromids’ foraging aggressiveness, therefore, affected not only the overall prey density but also resulted in different prey community composition. As pest density and composition can both affect crop performance, further research needs to investigate how the interindividual behavioral differences of generalist natural enemies cascade down on the crops.

Lack of phenotypic variation despite population structure in larval utilization of pea aphids by populations of the lady beetle Hippodamia convergens

The convergent lady beetle (Hippodamia convergens) is a generalist natural enemy that is utilized extensively in augmentative biological control across the United States. Recent studies have pointed to both genetic and phenotypic differences in Western (California) versus Eastern (Kansas) populations of the species. Here we investigate (1) genetic population structure, and (2) phenotypic differences in the utilization of pea aphids at temperatures that resemble the Western United States in (a) Eastern versus Western populations, (b) F1 Eastern X Western hybrids versus their progenitor populations, and investigate the effects of competition between (c) Eastern and Western populations. We found no differences in final pupal weight, or the net weight gain ratio through larval development from the third instar to pupal stage, despite genetic population structure. Our study points towards plastic response and effectiveness in feeding phenotypes of Eastern and Western populations of H. convergens, and the absence of hybrid vigor and heterozygote advantages in hybrids.

Forest cover and proximity decrease herbivory and increase crop yield via enhanced natural enemies in soybean fields

Abstract Non‐crop habitats are essential for sustaining biodiversity of beneficial arthropods in agricultural landscapes, which can increase ecosystem services provision and crop yield. However, their effects on specific crop systems are less clear, such as soybean in South America, where the responses of pests and natural enemies to landscape structure have only recently been studied. Here, we analysed how native forest fragments at local and landscape scales influenced arthropod communities, herbivory and yield in soybean fields in central Argentina. To do this, we selected soybean fields located in agricultural landscapes with varying proportions of forest cover. At two distances (10 and 100 m) from a focal forest fragment, we sampled natural enemy and herbivore arthropods, and measured soybean herbivory and yield. We focused on herbivore diversity, abundance of key soybean pests in the region (caterpillars and stink bugs), and their generalist and specialist natural enemies. Higher abundance of predators, lower herbivory rates and increased yield were found near forests, while overall forest cover in the landscape was positively related with parasitoid and stink bug abundance, soybean yield, and negatively with herbivory. Moreover, yield was positively linked to richness and abundance of generalist and specialist enemies and independent of herbivory according to piecewise Structural Equation Models. Synthesis and applications. Our results show positive effects of native forests on biodiversity and yield in soybean crops, highlighting the need for conservation of forest fragments in agricultural landscapes. Moreover, the relation between natural enemies and crop yield suggests that Chaco forests support a diverse and abundant community of natural enemies that can provide sustained levels of ecosystem services and result in positive effects for farmers.

A widespread interaction between generalist and specialist enemies: The role of intraguild predation and Allee effect

A natural food web system involves a diverse community of natural enemies and one of the widespread and common phenomena of such systems is intraguild predation (IGP) (i.e., presence of eating and killing among potential competitors). Here, we investigate the dynamics of a food web system with Allee effect and intraguild predation. In the present study, generalist and specialist natural enemies competing for a shared resource (prey) (intraguild predation) have been introduced. The Allee effect has also been incorporated in the shared prey growth rate. We investigate how parameters defining Allee effect and intraguild predation affect the long-term persistence, extinction and co-existence regions of such species. We outline the conditions under which different types of interior and non-interior equilibria exist and are locally stable. Bi-stable dynamics has also been investigated for the proposed model system for a suitable range of parametric values. A threshold condition on the strength of Allee effect has been obtained assuring the absence of IG predator population along with extinction region of shared prey. To understand the dynamics of the system, a comprehensive study of bifurcation analysis has also been provided taking Allee effect and fertility rate of intraguild predator as bifurcation parameters. These two parameters generate various interesting bifurcations like saddle-node bifurcation and Hopf-bifurcation. We have obtained different parametric regions of Allee parameter for the existence of different boundary and interior equilibria. All the analytical results related with local stability of equilibrium points and all possible successive bifurcations have been supported by different numerical examples, one and two parameter bifurcation diagrams, bi-stability diagram and stability regions of all possible equilibrium points. The impacts of Allee effect on co-existence, stability, extinction of species, their persistence, bistability and bifurcations have been explicitly discussed and the whole dynamics has also been successfully compared with the dynamics of food web without Allee effect. It is observed that the introduction of Allee effect and IG predator induce more rich dynamics and compel the system to be more sensitive to initial population densities.

The potential impact of climate change on non-target risks from imported generalist natural enemies and on biological control

Climate change creates opportunities and constraints for imported biological control agents, target pests, and non-target prey to modify their geographic distributions. However, predictions about how climate change will affect distributions of natural enemies and their hosts/prey cannot be made at present because of insufficient data about how species will respond to climate change, both directly and indirectly. Factors underlying the responses include tolerance to physical changes in the environment, dispersal ability, geography, and habitat requirements. Despite the limitations for making predictions, a review of the literature for imported generalist natural enemies indicates that climate change will result in range expansions or range shifts in some species, and that these changes are likely to increase non-target risks as well as influence the effectiveness of biological control programs. To better guide future decisions concerning importation biological control, additional field studies, experiments, and theoretical models are needed. Recommended actions include conducting surveys for non-target species in areas undergoing climate change, determining tolerances to changes in temperature and precipitation for natural enemies and hosts/prey, incorporating climate data into insect population models, and long-term assessments to document the impact of climate change on non-target species and efficacy of biological control programs. Because climate change will impact both target pests and non-target species, the work will be best-accomplished by grant-funded programs involving interdisciplinary teams of scientists.

Biodiversity of the natural enemies of aphids (Hemiptera: Aphididae) in Northwest Turkey

In the present study, the natural enemies of aphids (Hemiptera: Aphididae) and their host plants including herbaceous plants, shrubs and trees were analysed to reveal their biodiversity and disclose tritrophic associations in different habitats of the South Marmara region of northwest Turkey. As a result of field surveys, 58 natural enemy species associated with 43 aphids on 58 different host plants were identified in the region between March of 2017 and November of 2018. In 173 tritrophic natural enemy-aphid-host plant interactions including association records new for Europe and Turkey, there were 21 representatives of the family Coccinellidae (Coleoptera), 14 of the family Syrphidae (Diptera) and 15 of the subfamily Aphidiinae (Hymenoptera), as well as eight other generalist natural enemies. In these interactions, a total of 37 aphid-natural enemy associations–including 19 associations of Acyrthosiphon pisum (Harris) with natural enemies, 16 associations of Therioaphis trifolii (Monell) with natural enemies and two associations of Aphis craccivora Koch with natural enemies–were detected on Medicago sativa L. during the sampling period. Similarly, 12 associations of Myzus cerasi (Fabricius) with natural enemies were revealed on Prunus avium (L.), along with five associations of Brevicoryne brassicae (Linnaeus) with natural enemies (including mostly parasitoid individuals) on Brassica oleracea L. Also in the study, reduviids of the species Zelus renardii (Kolenati) are reported for the first time as new potential aphid biocontrol agents in Turkey. The results of field surveys show that the natural enemies of aphids have high biodiversity, which should be considered in the management of biological pest control.

Top-down pressure by generalist and specialist natural enemies in relation to habitat heterogeneity and resource availability

Habitat heterogeneity might promote the abundance and richness of natural enemies potentially leading to higher top-down pressure on herbivorous insects. Heterogeneous habitats could provide natural enemies with more abundant and alternative resources and a greater variety of micro-habitats. Natural enemies with different searching behaviours, e.g. generalists and specialists, could be affected in different ways by habitat heterogeneity, thus affecting their pressure on herbivorous insects.To understand how top-down pressure on herbivorous insects is promoted by habitat heterogeneity, it is crucial to investigate which parameters contributing to habitat heterogeneity affect not only the abundance and richness but also the searching behaviour of different natural enemies. We investigated the relationship between heterogeneity in forest habitats and the top-down pressure exerted by generalist predators and specialist parasitoids on larvae of the European pine sawfly (Neodiprion sertifer).We used forest stands with endemic or epidemic densities of resident sawfly populations. Within each stand we selected experimental trees to create variation in tree species diversity and density in their surrounding area, i.e. habitat heterogeneity. We found that a higher tree density increased the predation by generalists on sawfly larvae in stands with endemic sawfly densities. Parasitoids were less successful in stands with endemic sawfly densities. Total mortality depended on stand character and the proportion of pine around experimental trees.The explained variation in the response variables by the models is relatively low, indicating that other measures of heterogeneity, like understory vegetation and presence of dead wood could contribute to the observed variation. Also, interference between generalist and specialist enemies could affect the realized mortality pressure. Thus, the effect of tree species diversity in combination with these other measures of heterogeneity needs to be recognized to promote the presence and the activity of natural enemies in managed habitats.