Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

Hackett, Sean; Karley, Alison J.; Bennett, Alison E.

doi:10.1098/rspb.2013.1275

Cited by 21 publications

(21 citation statements)

References 33 publications

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“…The importance of species and genotype identity on trophic interactions has been demonstrated between insects and plants (Oliver, Moran & Hunter ; Bilodeau et al . ; Cayetano & Vorburger ; Hackett, Karley & Bennett ) and AM fungi and their host plants (Vandenkoornhuyse et al . ; Gange, Brown & Aplin ; Bennett, Alers‐Garcia & Bever ; Jansa, Smith & Smith ; Hempel et al .…”

Section: Discussionmentioning

confidence: 99%

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

et al. 2016

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Summary Understanding how soil microbial communities influence plant interactions with other organisms, and how this varies with characteristics of the interacting organisms, is important for multiple systems. Solanum spp. are a suitable model for trophic interactions in studies of agricultural and natural systems and can also provide useful corollaries in invaded systems. This study examined the influence of soil mutualist arbuscular mycorrhizal (AM) fungi on growth of different Solanum types fed on by the potato aphid, Macrosiphum euphorbiae, in relation to the presence of the aphid facultative endosymbiont Hamiltonella defensa. Four Solanum types comprising two wild species, S. berthaultii and S. polyadenum, and two accessions of S. tuberosum, were grown with or without AM fungi and infested with one of four clonal lines of a single M. euphorbiae genotype (two with and two without H. defensa). Two experiments were conducted to (i) characterize plant responses to AM fungi and aphids and (ii) assess whether soil AM fungi could influence the success of the parasitoid wasp Aphidius ervi when attacking aphids reared on each Solanum type. In both experiments, similar patterns of plant biomass were observed in relation to AM fungal and aphid treatments. Solanum biomass depended on plant type and aphid infection with H. defensa. Plants exposed to aphids harbouring H. defensa had smaller root biomass, and therefore total plant biomass, compared to plants infested with H. defensa‐free aphids. M. euphorbiae performance varied with aphid clonal line, Solanum type and the presence of AM fungi. Parasitoid success, measured as the proportion of aphids from which a wasp emerged, was highest from aphids that had fed on plants colonized by AM fungi, although this result also varied with Solanum type and aphid clonal line. Synthesis. The presence of soil AM fungi, combined with within‐species plant and insect variation in key traits, can have subtle – but significant – effects on plant fitness and insect success. This study highlights the importance of exploring genotypic variation in plant and pest responses to soil microbiota to identify suitable biocontrol options.

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Section: Discussionmentioning

confidence: 99%

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

et al. 2016

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“…Their fecundity was assessed for a duration equivalent to twice the prereproductive period duration (PRP) for each aphid species. Newly larviposited nymphs were removed daily (Hackett, Karley, & Bennett, 2013;Le Roux, Saguez, Vincent, & Giordanengo, 2004).…”

Section: Nitrogen Treatment and Aphid Performancementioning

confidence: 99%

Cascading effects of N input on tritrophic (plant–aphid–parasitoid) interactions

Chesnais

Couty

Catterou

et al. 2016

Ecology and Evolution

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Because N is frequently the most limiting mineral macronutrient for plants in terrestrial ecosystems, modulating N input may have ecological consequences through trophic levels. Thus, in agro‐ecosystems, the success of natural enemies may depend not only from their herbivorous hosts but also from the host plant whose qualities may be modulated by N input. We manipulated foliar N concentrations by providing to Camelina sativa plants three different nitrogen rates (control, optimal, and excessive). We examined how the altered host‐plant nutritional quality influenced the performances of two aphid species, the generalist green peach aphid, Myzus persicae, and the specialist cabbage aphid, Brevicoryne brassicae, and their common parasitoid Diaeretiella rapae. Both N inputs led to increased N concentrations in the plants but induced contrasted concentrations within aphid bodies depending on the species. Compared to the control, plant biomass increased when receiving the optimal N treatment but decreased under the excessive treatment. Performances of M. persicae improved under the optimal treatment compared to the control and excessive treatments whereas B. brassicae parameters declined following the excessive N treatment. In no‐choice trials, emergence rates of D. rapae developing in M. persicae were higher on both optimum and excessive N treatments, whereas they remained stable whatever the treatment when developing in B. brassicae. Size of emerging D. rapae females was positively affected by the treatment only when it developed in M. persicae on the excessive N treatment. This work showed that contrary to an optimal N treatment, when N was delivered in excess, plant suitability was reduced and consequently affected negatively aphid parameters. Surprisingly, these negative effects resulted in no or positive consequences on parasitoid parameters, suggesting a buffered effect at the third trophic level. Host N content, host suitability, and dietary specialization appear to be major factors explaining the functioning of our studied system.

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“…The potato aphid, Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae: Macrosiphini), is a common and highly polyphagous aphid infesting more than 200 plant species in natural and cropped vegetation in northern temperate regions, but despite its cosmopolitan nature, relatively little is known about variation within this species (Blackman & Eastop, ). Whereas H. defensa and R. insecticola have been detected in M. euphorbiae in the USA (Russell et al., ) and the UK (Hackett et al., ; Henry et al., ), the physiological effects of facultative endosymbionts on aphid fitness and susceptibility to parasitism remain largely uncharacterized. Macrosiphum euphorbiae provides a suitable model, therefore, to assess aphid‐ and endosymbiont‐mediated attributes influencing aphid fitness that is relevant to the ecology and population regulation of this and other polyphagous aphid species in natural and managed vegetation.…”

Section: Introductionmentioning

confidence: 99%

Susceptibility of Macrosiphum euphorbiae to the parasitoid Aphidius ervi: larval development depends on host aphid genotype

Clarke

Cullen

Hubbard

et al. 2016

Entomologia Exp Applicata

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The potato aphid, Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae: Macrosiphini), is a common polyphagous aphid in Europe and North America. However, the factors influencing potato aphid dynamics and susceptibility to natural enemies are largely undescribed, particularly in relation to facultative endosymbiotic bacteria, which can provide protection against parasitism and disease in some aphid species. This study investigated whether potato aphid susceptibility to one of its principal natural enemies, the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), varied in relation to aphid genotype and/or endosymbiont presence. Parasitism and aphid fitness assays were conducted on clonal lineages of aphids, harbouring their natural endosymbiont infections, collected over 3 years from separate geographic locations. Parasitized aphids were dissected to quantify parasitoid oviposition, larval development, and mummification. Amongst the 19 clonal lines of M. euphorbiae tested, seven aphid genotypes were identified, and 11 lines harboured one or both of the facultative endosymbionts Hamiltonella defensa Moran et al. and Regiella insecticola Moran et al.; H. defensa infections were associated exclusively with two of the seven M. euphorbiae genotypes. Par-asitism resistance was detected in clonal lines belonging to a single aphid genotype and resulted from failure of parasitoid eggs to develop into larvae rather than failure of the parasitoid to oviposit. Contrary with studies of several other aphid species, there was little evidence that H. defensa provided strong protection to M. euphorbiae from parasitism by A. ervi. Furthermore, there were no clear fitness costs to the aphid associated with parasitism resistance or with H. defensa infection. The two M. euphorbiae genotypes in which H. defensa occurred, which included the resistant genotype, exhibited faster development, higher survival, and greater fecundity than the other five aphid genotypes. These findings suggest that biological control of M. euphorbiae using A. ervi alone could exacerbate pest problems by selecting for the fittest parasitism-resistant genotypes.

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Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

Cited by 21 publications

References 33 publications

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

Cascading effects of N input on tritrophic (plant–aphid–parasitoid) interactions

Susceptibility of Macrosiphum euphorbiae to the parasitoid Aphidius ervi: larval development depends on host aphid genotype

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