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AbstractThe persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms' dependence on two dimensions of spatial structure-the initial spatial association of fungi and the ease of fungal dispersal-through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

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In mutualism, hosts select symbionts via partner choice and preferentially direct more resources to symbionts that provide greater benefits via sanctions. At the initiation of symbiosis, prior to resource exchange, it is not known how the presence of multiple symbiont options (i.e. the symbiont social environment) impacts partner choice outcomes. Furthermore, little research addresses whether hosts primarily discriminate among symbionts via sanctions, partner choice or a combination. We inoculated the legume, Acmispon wrangelianus, with 28 pairs of fluorescently labelled Mesorhizobium strains that vary continuously in quality as nitrogen-fixing symbionts. We find that hosts exert robust partner choice, which enhances their fitness. This partner choice is conditional such that a strain's success in initiating nodules is impacted by other strains in the social environment. This social genetic effect is as important as a strain's own genotype in determining nodulation and has both transitive (consistent) and intransitive (idiosyncratic) effects on the probability that a symbiont will form a nodule. Furthermore, both absolute and conditional partner choice act in concert with sanctions, among and within nodules. Thus, multiple forms of host discrimination act as a series of sieves that optimize host benefits and select for costly symbiont cooperation in mixed symbiont populations.

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BACKGROUND: Combining different biocontrol agents, particularly micro- and macroorganisms, can contribute to new and sustainable pest control approaches. Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is one of the most destructive pests of solanaceous crops. An emerging management strategy consists of biological control using microbial insecticides such as baculoviruses, but with limited efficacy. Thanks to their high target specificity, baculoviruses can be used simultaneously with natural enemies such as parasitoids for improved control of T. absoluta. However, potential indirect nontarget effects of baculoviruses on parasitoids can result from overlapping resource requirements. We assessed whether ovipositing parasitoid females discriminated against virus-treated hosts and examined the outcome of within-host competition between the hymenopteran parasitoids Necremnus tutae (Reuter) (Eulophidae) and Dolichogenidea gelechiidivoris Marsch (Braconidae), and the Phthorimaea operculella granulovirus (PhopGV, Baculoviridae) that infects T. absoluta larvae. RESULTS: Female D. gelechiidivoris discriminated against virus-treated hosts, whereas N. tutae did not. We found few indirect virus-related effects depending on the species, the sex, and the time of virus treatment. Effects were ambivalent for D. gelechiidivoris offspring and ranged from increased male longevity when infection occurred before parasitization to reduced emergence and male longevity when infection occurred after parasitization. N. tutae offspring showed a longer development time and shorter male longevity when they developed in virus-treated hosts. CONCLUSION: The virus had a low impact on parasitoid offspring. In rare cases, adverse effects were detected; however, the low magnitude of these effects is unlikely to reduce the fitness of parasitoid offspring, therefore both parasitoids seem compatible with the baculovirus for control of T. absoluta. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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In solitary endoparasitoids, oviposition in a host previously parasitized by a conspecific (superparasitism) leads to intraspecific competition, resulting in the elimination of all but one parasitoid offspring. Therefore, avoidance of parasitized hosts presents a strong selective advantage for such parasitoid species. Parasitoids use herbivore-induced plant volatiles (HIPVs) to find their hosts. In this study, we evaluated the ability of Microplitis croceipes (Hymenoptera: Braconidae) to discriminate between unparasitized and parasitized Heliothis virescens (Lepidoptera: Noctuidae) larvae using cotton plant odors as cues. A combination of behavioral and analytical techniques were used to test two hypotheses: (i) parasitoids will show preference for plant odors induced by unparasitized hosts over odors induced by parasitized hosts, and (ii) the parasitism status of herbivores affects HIPV emission in plants. Heliothis virescens larvae were parasitized for varying durations (0, 2 and 6-days after parasitism (DAP)). In four-choice olfactometer bioassays, female M. croceipes showed greater attraction to plant odors induced by unparasitized hosts compared to plant odors induced by parasitized hosts (2 and 6-DAP). Comparative gas chromatography-mass spectrometry analyses of cotton volatiles indicated reduced emission of 10 out of 21 identified compounds from plants infested by parasitized hosts compared with plants infested by unparasitized hosts. The results suggest that changes in plant volatile emission due to the parasitism status of infesting herbivores affect recruitment of parasitoids. Avoidance of superparasitism using plant odors optimizes host foraging in M. croceipes, and this strategy may be widespread in solitary parasitoid species.

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Cotton bollworm, Helicoverpa armigera Hubner, is a cosmopolitan polyphagous pest of many crops. Habrobracon hebetor Say and Helicoverpa armigera nucleopolyhedrovirus (HearNPV) are two important biocontrol agents used to manage this pest, sometimes in combination. We evaluated the sublethal effects of HearNPV on H. hebetor life table parameters under laboratory conditions when its host (second instar H. armigera) was treated with HearNPV, and tested H. hebetor females for their ability to discriminate against inoculated hosts. Emergence of adults reared as solitary larvae was reduced by half on LC30-inoculated larvae compared to controls, but not on LC5 or LC15-inoculated hosts. Low concentrations (LC5, LC15, and LC30) of HearNPV had no effects on overall parasitoid developmental time, but longevity and lifetime fecundity was reduced for females emerging from hosts receiving the LC30 treatment. Net reproductive rate (R0), intrinsic rate of increase (rm), and finite rate of increase (λ) were all decreased in a concentration-dependent manner in the LC15 and LC30 treatments, as were female life expectancy, age-specific survivorship (lx), and age-specific fecundity (mx), whereas population doubling time (DT) increased. Parasitoids did not discriminate against LC15-inoculated larvae in choice or no-choice tests, but parasitized more LC50-inoculated hosts than controls in the choice test, with no significant differences in total numbers of eggs laid in either case. Although parasitoids suffered some loss of fitness in HearNPV-inoculated hosts under these laboratory conditions, these agents still appear compatible for joint application against H. armigera under field conditions, provided parasitoid releases are made 2 d after NPV application.

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When attacked by herbivores, plants emit volatiles to attract parasitoids and predators of herbivores. However, our understanding of the effect of plant volatiles on the subsequent behaviour of conspecific parasitoids when herbivores on plants are parasitized is limited. In this study, rice plants were infested with gravid females of the brown planthopper (BPH) Nilaparvata lugens for 24 hr followed by another 24 hr in which the BPH eggs on plants were permitted to be parasitized by their egg parasitoid, Anagrus nilaparvatae; volatiles from rice plants that underwent such treatment were less attractive to subsequent conspecific parasitoids compared to the volatiles from plants infested with gravid BPH females alone. Chemical analysis revealed that levels of JA and JA-Ile as well as of four volatile compounds-linalool, MeSA, α-zingiberene and an unknown compound-from plants infested with BPH and parasitized by wasps were significantly higher than levels of these compounds from BPH-infested plants. Laboratory and field bioassays revealed that one of the four increased chemicals-α-zingiberene-reduced the plant's attractiveness to the parasitoid. These results suggest that host plants can fine-tune their volatiles to help egg parasitoids distinguish host habitats with parasitized hosts from those without.

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The use of multiple species in biological control programmes is controversial when interactions among them are not fully understood. We determined the response of the pupal parasitoid Coptera haywardi (Oglobin) to different availability of Anastrepha ludens (Loew) pupae previously parasitized or not by larval-pupal Diachasmimorpha longicaudata (Ashmead). The two types of pupae were exposed at different ages and proportions to different numbers of C. haywardi females for 48 h. The performance of C. haywardi adults emerging from parasitized and unparasitized pupae was measured. Coptera haywardi prefers to attack unparasitized A. ludens pupae rather than pupae parasitized by D. longicaudata. However, when the availability of unparasitized pupae was low or the number of foraging females was high, C. haywardi competed against early immature stages of the D. longicaudata, or hyperparasitized, feeding directly on the advanced-immature developmental stages of the early acting species. Adults of C. haywardi emerging as hyperparasitoids were no different in size, fecundity and longevity from those emerging as primary parasitoids. Our data suggest that simultaneous use of these species in augmentative biological control projects may be feasible but should be carefully planned in order to avoid any detrimental effect of its interaction.

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Superparasitism is an adaptive strategy in solitary parasitoids, yet insufficient evidence confirms this in gregarious ones. We here ask whether the gregarious parasitoid Oomyzus sokolowskii is able to discriminate in attack and progeny allocation between parasitized and unparasitized Plutella xylostella larvae, and how the parasitoid allocates brood size and sex to superparasitized hosts due to some circumstances. We found that female parasitoids preferred unparasitized to parasitized host larvae, and allocated a smaller brood with more males in the later than in the former host. Brood size and sex ratio decreased from superparasitized hosts with a 48 h interval since a previous attack compared with one without an interval; they also declined from the host superparasitized by the parasitoid with oviposition experience compared with one without it. Brood size and sex ratio did not differ between the host superparasitized by the same parasitoid as in the first attack and that by a different one. Our findings suggest that O. sokolowskii females may adjust their oviposition decisions on progeny allocation in response to parasitized P. xylostella larvae to maximize their fitness gains from superparasitism.

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Natal rearing experience of animals may affect their behaviors, such as habitat selection and oviposition decision. As part of the overall fitness of insect parasitoids, successful host discrimination (distinguishing parasitized hosts from unparasitized hosts) is of paramount importance. In this study we examined whether and how parasitoids' natal rearing experience would affect their host discrimination ability according to host availability. We established separate colonies of Aphidius gifuensis Ashmead by continual rearing on two hosts, Sitobion avenae F. and Myzus persicae (Suzler), and quantified self superparasitism and self superparasitism versus parasitism ratio for the four combinations of parasitoid colonies and host species (S. aveane and M. persicae) at four host densities (30, 50, 100 or 150 per plant). Results showed that self superparasitism of M. persicae by A. gifuensis reared on S. avenae was significantly higher than by those reared on M. persicae, no matter whether the host densities were 30, 50, 100 or 150. Aphidius gifuensis reared on M. persicae significantly superparasitized more S. avenae than those reared on S. aveane only when host density was 30. Self superparasitism versus parasitism ratio of A. gifuensis from both colonies was always lower on natal hosts than on new hosts, and the difference was more pronounced as the host density decreased. These results suggested that natal rearing effects is important on host discrimination and oviposition decision of the parasitoid A. gifuensis. These effects promoted the parasitoid's host adaptation and made them confer greater fitness.

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BACKGROUND: Anopheles arabiensis is a dominant vector of malaria in sub-Saharan Africa, which feeds indoors and outdoors on human and other vertebrate hosts, making it a difficult species to control with existing control methods. Novel methods that reduce human-vector interactions are, therefore, required to improve the impact of vector control programmes. Investigating the mechanisms underlying the host discrimination process in An. arabiensis could provide valuable knowledge leading to the development of novel control technologies. In this study, a host census and blood meal analysis were conducted to determine the host selection behaviour of An. arabiensis. Since mosquitoes select and discriminate among hosts primarily using olfaction, the volatile headspace of the preferred non-human host and non-host species, were collected. Using combined gas chromatography and electroantennographic detection analysis followed by combined gas chromatography and mass spectrometry, the bioactive compounds in the headspace collections were identified. The efficiency of the identified non-host compounds to repel host-seeking malaria mosquitoes was tested under field conditions. RESULTS: The host census and blood meal analyses demonstrated that An. arabiensis strongly prefers human blood when host seeking indoors, while it randomly feeds on cattle, goats and sheep when found outdoors. However, An. arabiensis avoids chickens despite their relatively high abundance, indicating that chickens are a non-host species for this vector. Eleven bioactive compounds were found in the headspace of the non-host species. Six of these were species-specific, out of which four were identified using combined gas chromatography and mass spectrometry. When tested in the field, the chicken-specific compounds, isobutyl butyrate, naphthalene, hexadecane and trans-limonene oxide, and the generic host compounds, limonene, cis-limonene oxide and ß-myrcene, significantly reduced trap catches within the house compared to a negative control. A significant reduction in trap catch was also observed when suspending a caged chicken next to the trap. CONCLUSIONS: Non-host volatiles repel host-seeking An. arabiensis and thus play a significant role in host discrimination. As such, this study demonstrates that non-host volatiles can provide protection to humans at risk of mosquito-vectored diseases in combination with established control programmes.

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Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) is an important natural enemy of many species of lepidopterous pests and a widely used biological control agent. Detailed knowledge about its mate choice and host discrimination behavior is lacking. In this study, we studied the mate choice and host discrimination behavior of T. chilonis in experimental arenas through video tracking. Males' mate recognition capacity was realized by perceiving the sex pheromone of females. When offered two females of different species, male could distinguish the conspecific female from Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae), a species that has overlapping hosts with T. chilonis. When placed with two females of different mating status, male preferred mating with the virgin female to the mated female. T. chilonis females could distinguish unparasitized host eggs from parasitized ones (parasitized by conspecific females or heterospecific females). They preferred to stay on and lay eggs in unparasitized host eggs. When T. chilonis females were only provided with parasitized host eggs (parasitized by T. chilonis and T. bactrae females), conspecific superparasitism occurred more often than heterospecific superparasitism. Furthermore, the host egg discrimination ability of T. chilonis females was mainly achieved through antennal perception.

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Two generalist parasitoids, Dolichogenidea tasmanica (Cameron) (Hymenoptera: Braconidae) and Therophilus unimaculatus (Turner) (Hymenoptera: Braconidae) attack early instars of tortricid moths, including the light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae). The two parasitoids co-exist in natural habitats, while D. tasmanica is dominant in vineyards, whereas T. unimaculatus occurs mainly in adjacent native vegetation. This difference suggests possible competition between the two species, mediated by habitat. Here, we report on the extent of interspecific differences in host discrimination and the outcome of interspecific competition between the two parasitoids. The parasitoids did not show different behavioural responses to un-parasitized hosts or those that were parasitized by the other species. Larvae of D. tasmanica out-competed those of T. unimaculatus, irrespective of the order or interval between attacks by the two species. The host larvae that were attacked by two parasitoids died more frequently before a parasitoid completed its larval development than those that were attacked by a single parasitoid. Dissection of host larvae parasitized by both species indicated that first instars of D. tasmanica attacked and killed larval T. unimaculatus.

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Two laboratory experiments were conducted to examine the ovipositional preferences of the egg parasitoidOoencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) for parasitized and unparasitizedMegacopta punctatissimum Montandon (Hemiptera: Plataspidae). Females that had never oviposited or that had not oviposite for 3 days preferred recently parasitized hosts more than unparasitized hosts. The preference for recently parasitized hosts appeared to be mediated by the punctures in already parasitized hosts made by the ovipositor of the first female. Survival of the parasitoid progeny was lower in recently parasitized hosts than in unparasitized hosts. However, handling time of parasitized hosts was extremely short relative to that of unparasitized hosts, because the superparasitizing female could use the punctures made by the previous females. It is concluded that the females preferred the parasitized hosts over unparasitized hosts because the benefit of saving time and energy for drilling was more than the cost of progeny survival.