Sublethal effects of beta-cypermethrin modulate interspecific interactions between specialist and generalist aphid species on soybean.

In agroecosystems, plant-pest interactions are at the basis of complex food webs, which can be affected by both biotic and abiotic factors. In the present study, we evaluated the impact of the insecticide beta-cypermethrin on interspecific interactions between the specialist aphid Aphis glycines and the generalist aphid Aulacorthum solani on soybean. Aphis glycines showed higher fecundity than A. solani on soybean and the aphids caused unbalanced reduction in population growth on each other. A sublethal concentration of beta-cypermethrin (LC5 for A. glycines) stimulated the reproduction of A. glycines but it did not impact the fecundity of A. solani. However, the LC5 of beta-cypermethrin enhanced the interspecific inhibition of fecundity between the two aphid species. Moreover, the two species showed different spatial distribution on soybean seedlings. Aphis glycines mainly aggregated on the stem of soybean plant while A. solani colonized soybean leaves. The LC5 of beta-cypermethrin drove A. solani migrating from soybean leaves to stems independently of interspecific competition. Aphis glycines facilitated A. solani colonization on soybean plant through impacting host susceptibility, and vice versa. Nevertheless, such facilitated colonization-induced susceptibility could be modulated through exposure to the LC5 of beta-cypermethrin. These findings hinted that the pyrethroid insecticide beta-cypermethrin has the potential to mediate the interspecific competition between specialist and generalist aphids (at the sublethal concentration of LC5), and that it could influence aphid population growth and community structure in soybean crops. This knowledge could contribute to rationalize application of insecticides and to optimize Integrated Pest Management in soybean.

Individual flowering phenology shapes plant-pollinator interactions across ecological scales affecting plant reproduction.

The balance of pollination competition and facilitation among co-flowering plants and abiotic resource availability can modify plant species and individual reproduction. Floral resource succession and spatial heterogeneity modulate plant-pollinator interactions across ecological scales (individual plant, local assemblage, and interaction network of agroecological infrastructure across the farm). Intraspecific variation in flowering phenology can modulate the precise level of spatio-temporal heterogeneity in floral resources, pollen donor density, and pollinator interactions that a plant individual is exposed to, thereby affecting reproduction. We tested how abiotic resources and multi-scale plant-pollinator interactions affected individual plant seed set modulated by intraspecific variation in flowering phenology and spatio-temporal floral heterogeneity arising from agroecological infrastructure. We transplanted two focal insect-pollinated plant species (Cyanus segetum and Centaurea jacea, n = 288) into agroecological infrastructure (10 sown wildflower and six legume-grass strips) across a farm-scale experiment (125 ha). We applied an individual-based phenologically explicit approach to match precisely the flowering period of plant individuals to the concomitant level of spatio-temporal heterogeneity in plant-pollinator interactions, potential pollen donors, floral resources, and abiotic conditions (temperature, water, and nitrogen). Individual plant attractiveness, assemblage floral density, and conspecific pollen donor density (C. jacea) improved seed set. Network linkage density increased focal species seed set and modified the effect of local assemblage richness and abundance on C. segetum. Mutual dependence on pollinators in networks increased C. segetum seed set, while C. jacea seed set was greatest where both specialization on pollinators and mutual dependence was high. Abiotic conditions were of little or no importance to seed set. Intra- and interspecific plant-pollinator interactions respond to spatio-temporal heterogeneity arising from agroecological management affecting wild plant species reproduction. The interplay of pollinator interactions within and between ecological scales affecting seed set implies a co-occurrence of pollinator-mediated facilitative and competitive interactions among plant species and individuals.

L'équilibre des relations de compétition et de facilitation entre plantes pour la pollinisation et la disponibilité des ressources abiotiques affectent le succès reproducteur des espèces et des individus de plantes. La succession temporelle et l'hétérogénéité spatiale des ressources florales modifient les interactions plantes­pollinisateurs à différentes échelles écologiques (individu végétal, assemblage plantes­pollinisateurs local, réseau d'interactions des infrastructures écologiques à travers la ferme). Les variations intraspécifiques de phénologie de floraison peuvent moduler le succès reproducteur individuel en déterminant le niveau d'hétérogénéité spatio­temporelle de densité de donneurs de pollen, des interactions plantes­pollinisateurs et des ressources florales auxquelles un individu de plante est exposé. Nous avons mené une expérimentation pour tester comment la production de graines des plantes sauvages est affectée par les interactions plantes­pollinisateurs à différentes échelles écologiques, ces interactions étant modulées par la phénologie florale et l'hétérogénéité spatio­temporelle des ressources florales (découlant des infrastructures agroécologiques). Nous avons transplanté 144 individus de deux espèces végétales entomophiles (Cyanus segetum et Centaurea jacea) dans des infrastructures agroécologiques (10 bandes fleuries et six bandes enherbées semées) d'un domaine agroécologique expérimental (125 ha). Ces espèces à phénologie de floraison contrastée présentent toutes deux une longue période de floraison avec des variations intraspécifiques qui déterminent l'exposition des individus aux interactions plantes­pollinisateurs et aux conditions météorologiques. Nous avons appliqué une approche phénologiquement explicite centrée sur l'individu végétal, de manière à relier précisément la période de floraison de chaque individu aux niveaux correspondants d'hétérogénéité spatio­temporelle des interactions plantes­pollinisateurs, des densités de donneurs de pollen potentiels, des ressources florales (aux échelles de l'individu végétal, de l'assemblage local et du réseau d'interactions des infrastructures écologiques à travers la ferme) et des conditions abiotiques (température, précipitations, azote). L'attractivité individuelle (offre florale et taux de visite par les pollinisateurs) ainsi que la densité florale (toutes espèces) dans l'assemblage interspécifique local ont affecté positivement la production individuelle de graines des deux espèces végétales. Celle de C. jacea augmentait aussi directement avec la densité d'individus conspécifiques fleuris dans l'assemblage local. La densité de couplage du réseau a affecté positivement la production individuelle de graines des deux espèces et a influencé celle de C. segetum en modifiant l'effet de l'assemblage local (richesse et densité florales, richesse spécifique de pollinisateurs potentiels) sur le nombre de graines par individu. Le succès reproducteur individuel de C. segetum augmentait aussi avec le niveau de dépendance mutuelle entre l'espèce et ses pollinisateurs dans le réseau. Chez C. jacea, la production de graines individuelle était maximisée quand à la fois le niveau de spécialisation de C. jacea sur ses pollinisateurs dans le réseau et sa dépendance mutuelle à ses pollinisateurs étaient élevés. Les conditions abiotiques n'ont eu qu'un impact limité voire inexistant sur le succès reproducteur. Nos résultats montrent comment l'équilibre des interactions plantes­pollinisateurs entre espèces et individus, peut répondre à l'hétérogénéité spatio­temporelle liée à la gestion agroécologique de différentes façons qui affectent la reproduction des plantes sauvages. Les relations entre les interactions plantes­pollinisateurs et la production individuelle de graines des plantes focales se déclinent entre et au sein de différentes échelles écologiques, de l'individu à la communauté, impliquant une co­occurrence d'interactions facilitatrices et compétitrices entre espèces et individus de plantes via les pollinisateurs.

Parasitism and Suitability of Trichogramma chilonis on Large Eggs of Two Factitious Hosts: Samia cynthia ricini and Antheraea pernyi.

Trichogramma, an effective biological control agent, demonstrates promise in environmentally sustainable pest management through its parasitic action toward insect eggs. This study evaluates the parasitism fitness and ability of T. chilonis with regard to two factitious host eggs, aiming to develop a cost-effective biological control program. While T. chilonis demonstrated the ability to parasitize both host eggs, the results indicate a preference for ES eggs over COS eggs. The parasitism and emergence rates of T. chilonis regarding ES eggs (parasitism: 89.3%; emergence: 82.6%) surpassed those for COS eggs (parasitism: 74.7%; emergence: 68.8%), with a notable increase in the number of emergence holes observed in the ES eggs compared to the COS eggs. Moreover, the developmental time of T. chilonis for ES eggs (10.8 days) was shorter than that for COS eggs (12.5 days), resulting in a lower number of dead wasps produced. Notably, no significant difference was observed in the female ratios between the two species. A comprehensive analysis was conducted, comparing the size and shell thickness of the two factitious hosts. The ES eggs exhibited smaller dimensions (length: 1721.5 µm; width: 1178.9 µm) in comparison to the COS eggs (length: 2908.8 µm; width: 2574.4 µm), with the ES eggshells being thinner (33.8 µm) compared to the COS eggshells (47.3 µm). The different host species had an effect on the body length of the reared parasitoids, with T. chilonis reared on COS hosts exhibiting a larger body length (female: 626.9 µm; male: 556.7 µm) than those reared on ES hosts (female: 578.8 µm; male: 438.4 µm). Conclusively, the results indicate that ES eggs present a viable alternative to COS eggs for the mass production of Trichogramma species in biological control programs.

Gradually Increasing the Temperature Reduces the Diapause Termination Time of Trichogramma dendrolimi While Increasing Parasitoid Performance.

Trichogramma dendrolimi Matsumura is widely used as a biological control agent of many lepidopteran pests. Diapause has been used as an effective method to preserve the Trichogramma products during mass rearing production. However, it currently takes at least 70 days to break diapause, and we tested whether gradually increasing the temperature instead of using constant temperature could reduce the time of diapause termination and offer a higher flexibility to Trichogramma producers. The diapause termination rates of individuals kept at different conditions were measured, and five groups for which diapause termination rate reached the 95% were selected to test five biological parameters, including the number of eggs parasitized, the parasitism and emergence rates, the female sex ratio, the wing deformation rate, and the parasitoid longevity. Compared to the currently used procedure (70 days at 3 °C), treatments with at least two different temperatures resulted in higher parasitism and emergence rates while keeping the other parameters constant. The treatment that consisted of at least two different temperatures preceded by only 55 days of induction period had the highest population trend index, meaning that the population under these conditions grows more rapidly. Our results demonstrate that gradually increasing temperature allows T. dendrolimi to complete diapause earlier than at present while increasing its potential pest control capacity and providing additional flexibility in mass production of T. dendrolimi.

Parasitoid-mediated indirect interactions between unsuitable and suitable hosts generate apparent predation in microcosm and modeling studies.

Parasitoids used as biological control agents often parasitize more than a single host species and these hosts tend to vary in suitability for offspring development. The population dynamics of parasitoids and hosts may be altered by these interactions, with outcomes dependent on the levels of suitability and acceptance of both host species. Parasitism of individuals of an unsuitable host species may indirectly increase populations of a suitable host species if eggs laid into unsuitable hosts do not develop into adult parasitoids. In this case, the unsuitable host is acting as an egg sink for parasitoids and this can reduce parasitism of suitable hosts under conditions of egg limitation. We studied parasitoid-mediated indirect interactions between two aphid hosts, Aphis glycines (the soybean aphid) and A. nerii (the milkweed, or oleander aphid), sharing the parasitoid Aphelinus certus. While both of these aphid species are accepted by A. certus, soybean aphid is a much more suitable host than milkweed aphid is. We observed a drastic reduction of parasitoid offspring production (45%) on the suitable host in the presence of the unsuitable host in microcosm assays. Aphelinus certus females laid eggs into the unsuitable hosts (Aphis nerii) in the presence of the suitable host leading to egg and/or time limitation and reduced fitness. The impact of these interactions on the equilibrium population sizes of the three interacting species was analyzed using a consumer-resource modeling approach. Both the results from the laboratory experiment and the modeling approaches identified apparent predation between soybean aphid and milkweed aphid, in which milkweed aphid acts as a sink for parasitoid eggs leading to an increase in the soybean aphid population. The presence of soybean aphids had the opposite effect on milkweed aphid populations as it supported increases in parasitoid abundance and thus reduced the fitness and abundance of this aphid species.

Combination of generalist predators, Nesidiocoris tenuis and Macrolophus pygmaeus, with a companion plant, Sesamum indicum: What benefit for biological control of Tuta absoluta?

Tuta absoluta is one of the most damaging pests of tomato crops worldwide. Damage due to larvae may cause up to 100% loss of tomato production. Use of natural enemies to control the pest, notably predatory mirids such as Nesidiocoris tenuis and Macrolophus pygmaeus, is increasingly being promoted. However, considering the potential damage caused to tomatoes by these omnivorous predators in the absence of T. absoluta, an alternative solution could be required to reduce tomato damage and improve the predators' performance. The use of companion plants can be an innovative solution to cope with these issues. The present study aimed to determine the influence of companion plants and alternative preys on the predators' performance in controlling T. absoluta and protecting tomato plants. We evaluated the effect of predators (alone or combined) and a companion plant (sesame (Sesamum indicum)) on T. absoluta egg predation and crop damage caused by N. tenuis. The influence of an alternative prey (Ephestia kuehniella eggs) on the spatial distribution of predators was also evaluated by caging them in the prey presence or absence, either on tomato or sesame plants or on both. We found that the presence of sesame did not reduce the efficacy of N. tenuis or M. pygmaeus in consuming T. absoluta eggs; hatched egg proportion decreased when N. tenuis, M. pygmaeus, or both predators were present. More specifically, this proportion was more strongly reduced when both predators were combined. Sesame presence also reduced necrotic rings caused by N. tenuis on tomato plants. Nesidiocoris tenuis preferred sesame over tomato plants (except when food was provided only on the tomato plant) and the upper part of the plants, whereas M. pygmaeus preferred tomato to sesame plants (except when food was provided only on the sesame plant) and had no preference for a plant part. Combination of predators N. tenuis and M. pygmaeus allows for better coverage of cultivated plants in terms of occupation of different plant parts and better regulation of T. absoluta populations. Sesamum indicum is a potential companion plant that can be used to significantly reduce N. tenuis damage to tomatoes.

Oviposition preference and adult performance of the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae): effect of leaf microstructure associated with ladybeetle attachment ability.

BACKGROUND: The leaf surface microstructure can greatly influence predator feeding behavior. However, its effects on predator oviposition preference, which is crucial for arthropod fitness at the population level, are largely unknown. This study aimed to test leaf discs and plants of five common host plant species of Bemisia tabaci, including Chinese kale, cotton, cucumber, eggplant, and sweetpotato, to determine the oviposition preference and offspring and adult performance of the whitefly predator Serangium japonicum. Cannibalism risk, attachment force, microstructure of the abaxial leaf surface (ALS), and ladybeetle tarsal morphology were examined. RESULTS: Ladybeetle's oviposition preference had no correlation with offspring performance but positively correlated with fecundity. Further, oviposition preference to leaf discs and fecundity positively correlated with attachment force. The cannibalism risk was not significantly different between plant species. The ALS of Chinese kale and eggplant supported the smallest and the largest attachment forces, respectively. The first one had epicuticular wax crystals, whereas the latter had stellate trichomes. The ALS of cotton and sweetpotato did not bear wax crystals or long trichomes. Cucumber leaves were covered with tapered trichomes. Tenant setae on the distal second tarsomere and a pair of curved, tapered claws on the distal fourth tarsomere were the attachment structures of S. japonicum, which interacted with the plant surface structures and generated the attachment force. CONCLUSION: Plant morphological traits, associated with ladybeetle attachment force and adult performance might be key factors in ladybeetle oviposition preference, and are expected to occur in other host plant herbivore-predator systems.

Impact of host endosymbionts on parasitoid host range - from mechanisms to communities.

In insects, bacterial endosymbionts are known to influence the ecology of their hosts by modifying interactions with natural enemies such as parasitoids. Symbionts can modulate both parasitoid behavioral and/or physiological traits as well as host behaviors and life-history traits. Together these suggest that endosymbionts may impact the host range of parasitoids. For example, endosymbionts may narrow parasitoid host range through first, reducing parasitoid ability to locate hosts and/or larval survival, second, affecting fitness traits of the emerging adult parasitoid and/or third, modulating the outcome of interference and exploitative competition between parasitoid species. From both a fundamental and applied point of view, these symbiotic effects would influence the ecology and evolution of parasitoids and associated population-level processes and ecosystem services (e.g. biocontrol).

The preference-performance relationship as a means of classifying parasitoids according to their specialization degree.

Host range in parasitoids could be described by the preference-performance hypothesis (PPH) where preference is defined as host acceptance and performance is defined as the sum of all species on which parasitoid offspring can complete their life cycle. The PPH predicts that highly suitable hosts will be preferred by ovipositing females. However, generalist parasitoids may not conform to this hypothesis if they attack a large range of hosts of varying suitability. Under laboratory conditions, we tested the PPH relationship of three aphid parasitoids currently considered as generalist species (Aphelinus abdominalis, Aphidius ervi, Diaeretiella rapae). As expected, the three parasitoids species showed low selectivity, i.e., females stung all aphid species encountered (at least in some extent). However, depending on the parasitoid species, only 42%-58% of aphid species enabled producing parasitoid offspring. We did not find a correlation between the extent of preference and the performance of three generalist aphid parasitoids. For A. ervi, host phylogeny is also important as females showed higher attack and developmental rates on hosts closely related to the most suitable one. In addition, traits such as (a) the presence of protective secondary endosymbionts, for example, Hamiltonella defensa detected in Aphis fabae and Metopolophium dirhodum and (b) the sequestration of plant toxins as defense mechanism against parasitism, for example, in Aphis nerii and Brevicoryne brassicae, were likely at play to some extent in narrowing parasitoid host range. The lack of PPH relationship involved a low selectivity leading to a high adaptability, as well as selection pressure; the combination of which enabled the production of offspring in a new host species or a new environment. Testing for PPH relationships in parasitoids may provide useful cues to classify parasitoids in terms of specialization degree.

Potential for insecticide-mediated shift in ecological dominance between two competing aphid species.

Competition is a key structuring component of biological communities, which is affected by both biotic and abiotic environmental stressors. Among the latter, anthropic stressors and particularly pesticides are noteworthy due to their intrinsic toxicity and large use in agroecosystems. However this issue has been scarcely documented so far. In this context, we carried out experiments under laboratory conditions to evaluate stress imposed by the neonicotinoid insecticide imidacloprid on intra and interspecific competition among two major wheat pest aphids. The bird cherry-oat aphid Rhopalosiphum padi L. and the English grain aphid Sitobion avenae F. were subjected to competition on wheat seedlings under varying density combinations of both species and subjected or not to imidacloprid exposure. Intraspecific competition does take place without insecticide exposure, but so does interspecific competition between both aphid species with R. padi prevailing over S. avenae. Imidacloprid interfered with both intra and interspecific competition suppressing the former and even the latter for up to 14 days, but not afterwards when a shift in dominance takes place favoring S. avenae over R. padi, in contrast with the interspecific competition without imidacloprid exposure. These findings hinted that insecticides are indeed able to mediate species interaction and competition influencing community structure and raising management concerns for favoring potential secondary pest outbreaks.