Interrelated effects of mycorrhiza and free‐living nitrogen fixers cascade up to aboveground herbivores

Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen‐fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co‐occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant‐associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free‐living nitrogen‐fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two‐spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co‐occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant‐mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.     

Trait‐mediated indirect interactions: Moose browsing increases sawfly fecundity through plant‐induced responses

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Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in <Emphasis Type="Italic">Vicia faba</Emphasis>

Arbuscular mycorrhizal fungi (AMF) can alter the physiology and morphology of their host plant, and therefore may have indirect effects on insect herbivores and pollinators. We conducted this study to test the hypothesis that AMF can also affect insects involved in protection-for-food mutualisms. We examined the constitutive and inducible production of food rewards [extrafloral (EF) nectaries] in Vicia faba plants by manipulating the presence/absence of AMF and by simulating various levels of herbivory. Plants inoculated with AMF produced significantly fewer EF nectaries than uninoculated plants, even after accounting for differences in plant growth. In contrast to earlier studies, EF nectaries were not inducible: damaged plants produced significantly fewer EF nectaries than undamaged plants. Moreover, the effects of mycorrhizal and damage status on EF nectary production were additive. The reduction in EF nectaries in mycorrhizal plants potentially represents a mechanism for indirect effects of AMF on the protective insects that exploit EF nectaries as a food source (e.g., ants). Reduced reward size should result in reduced protection by ants, and could therefore be a previously unappreciated cost of the mycorrhizal symbiosis to host plants. However, the overall effect of AMF will depend upon the extent to which the reduction of EF nectaries affects the number and activity of ants and the extent to which AMF alter other aspects of host plant physiology. Our results emphasize the complexity of multitrophic interactions, particularly those that span belowground and aboveground ecology.     

Genetic factors affecting food‐plant specialization of an oligophagous seed predator

Several ecological and genetic factors affect the diet specialization of insect herbivores. The evolution of specialization may be constrained by lack of genetic variation in herbivore performance on different food‐plant species. By traditional view, trade‐offs, that is, negative genetic correlations between the performance of the herbivores on different food‐plant species favour the evolution of specialization. To investigate whether there is genetic variation or trade‐offs in herbivore performance between different food plants that may influence specialization of the oligophagous seed‐eating herbivore, Lygaeus equestris (Heteroptera), we conducted a feeding trial in laboratory using four food‐plant species. Although L. equestris is specialized on Vincetoxicum hirundinaria (Apocynaceae) to some degree, it occasionally feeds on alternative food‐plant species. We did not find significant negative genetic correlations between mortality, developmental time and adult biomass of L. equestris on the different food‐plant species. We found genetic variation in mortality and developmental time of L. equestris on some of the food plants, but not in adult biomass. Our results suggest that trade‐offs do not affect adaptation and specialization of L. equestris to current and novel food‐plant species, but the lack of genetic variation may restrict food‐plant utilization. As food‐plant specialization of herbivores may have wide‐ranging effects, for instance, on coevolving plant–herbivore interactions and speciation, it is essential to thoroughly understand the factors behind the specialization process. Our findings provide valuable information about the role of genetic factors in food‐plant specialization of this oligophagous herbivore.     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

The effects of drought and herbivory on plant–herbivore interactions across 16 soybean genotypes in a field experiment

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Increased nutrient availability decreases insect resistance in cranberry

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Plant‐mediated effects of host plant density on a specialist herbivore of Solanum carolinense

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A plant pathogen causes extensive mortality in an invasive insect herbivore

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Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant–herbivore interaction

1. While both arbuscular mycorrhizal (AM) fungi and plant and insect genotype are well known to influence plant and herbivore growth and performance, information is lacking on how these factors jointly influence the relationship between plants and their natural herbivores. 2. The aim of the present study was to investigate how a natural community of arbuscular mycorrhizal fungi affects the growth of the perennial herb Plantago lanceolata L. (Plantaginaceae), as well as its interaction with the Glanville fritillary butterfly [Melitaea cinxia L. (Nymphalidae)]. For this, a multifactorial experiment was conducted using plant lines originating from multiple plant populations in the Åland Islands, Finland, grown either with or without mycorrhizal fungi. For a subset of plant lines, the impact of mycorrhizal inoculation, plant line, and larval family on the performance of M. cinxia larvae were tested. 3. Arbuscular mycorrhizal inoculation did not have a consistently positive or negative impact on plant growth or herbivore performance. Instead, plant genetic variation mediated the impact of arbuscular mycorrhizal fungi on plant growth, and both plant genetic variation and herbivore genetic variation mediated the response of the herbivore. For both the plant and insect, the impact of the arbuscular mycorrhizal community ranged from mutualistic to antagonistic. Overall, the present findings illustrate that genetic variation in response to mycorrhizal fungi may play a key role in the ecology and evolution of plant–insect interactions.     

The nutritional landscape of host plants for a specialist insect herbivore

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Dual colonization of Eucalyptus urophylla S.T. Blake by arbuscular and ectomycorrhizal fungi affects levels of insect herbivore attack

Abstract 1 Eucalypts are an important part of plantation forestry in Asia but, in south China, productivity is very low. This is due to infertile soils and lack of indigenous symbiotic mycorrhizal fungi. The genus Eucalyptus is unusual because it forms both arbuscular (AM) and ectomycorrhizal (ECM) associations. 2 Eucalyptus urophylla saplings were grown with and without AM (Glomus caledonium) and ECM (Laccaria laccata) fungi in a factorial design. Two experiments were performed: one to simulate nursery conditions and the other to simulate the early stages of plantation establishment. Plant growth was measured over 18 weeks and levels of insect attack were recorded. 3 The AM fungus reduced tree growth in the early stages, but the effect appeared to be transient. No effects of ECM were detected on tree growth, but the ectomycorrhiza reduced colonization by the arbuscular mycorrhiza. AM fungi appear to be rapid invaders of the root system, gradually being replaced by ECM. 4 Both fungal types affected levels of damage by insect herbivores. Most importantly, herbivory by the pest insects Anomala cupripes (Coleoptera) and Strepsicrates spp. (Lepidoptera) was decreased by ECM. 5 It is suggested that mycorrhizal effects on eucalypt insects may be determined by carbon allocation within the plant. Future studies of eucalypt mycorrhizas need to take into account the effects of the fungi on foliar‐feeding insects and also the effects of insect herbivory on mycorrhizal establishment.     

Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems

• 1 Below‐ground organisms influence above‐ground interactions in both natural and agricultural ecosystems. Among the most important below‐ground organisms are mycorrhizal fungi, comprising ubiquitous and ancient plant mutualists that have significant effects on plant growth and fitness mediated by resource exchange with plants. In the present study, we focus on the effects of arbuscular mycorrhizal fungi (AMF) on crop defence against insect pests.
• 2 AMF alter the availability of resources used by crop plants to manufacture defences against pests and to compensate for pest damage. However, AMF also provide plants with nutrients that are known to increase insect performance. Through potentially opposing effects on plant nutritional quality and defence, mycorrhizal fungi can positively or negatively affect pest performance.
• 3 Additionally, AMF may directly affect gene expression and plant defence signalling pathways involved in the construction and induction of plant defences, and these effects are apparently independent of those caused by nutrient availability. In this way, AMF may still influence plant defences in the fertilized and highly managed systems typical of agribusiness.
• 4 Because AMF can affect plant tolerance to pest damage, they may have a significant impact on the shape of damage–yield relationships in crops. Potential mechanisms for this effect are suggested.
• 5 We highlight the need for continuing research on the effects of AMF identity and the abundance on crop defences and tolerance to pest attack. Much work is needed on the potential effects of mycorrhizal colonization on plant signalling and the induction of direct and indirect defences that may protect against pest damage.

     

Stress magnitude matters: different intensities of pulsed water stress produce non‐monotonic resistance responses of host plants to insect herbivores

Abstract 1. Water stress may increase or reduce the suitability of plants for herbivores. The recently proposed ‘pulsed stress hypothesis’ suggests consideration of stress phenology (pulsed vs. continuous stress) to explain these conflicting effects of plant water stress on herbivore performance. 2. This hypothesis was tested for the effect of differing stress intensity on performance and preference of insect herbivores belonging to different feeding guilds, namely leaf‐chewing insects (Spodoptera littoralis caterpillars) and phloem‐feeding insects (Aphis pomi aphids), on apple plants (Malus domestica). The plants were non‐stressed or exposed to a low or high intensity of pulsed water stress. 3. Plant responses to the different stress levels were generally monotonic. Growth, stomatal conductance (g_s), leaf water, and old‐leaf nitrogen concentration decreased, whereas young‐leaf nitrogen concentration and leaf mass per area (LMA) increased with increasing stress intensity. The stable isotope composition of foliar carbon (δ¹³C) responded non‐monotonically to the drought treatments. The δ¹³C values were highest in low‐stress plants, intermediate in high‐stress plants, and lowest in non‐stressed plants. 4. The preference and performance responses of the caterpillars were also non‐monotonic. Non‐stressed plants were intermediately, low‐stress plants least, and high‐stress plants most attractive or suitable. Aphid population growth was highest on non‐stressed plants and lowest on low‐stress plants. 5. The results highlight the importance of water stress intensity for the outcome of interactions between herbivores and drought‐affected plants. They show that pulsed water stress may enhance or reduce insect herbivore performance and plant resistance, depending on stress intensity.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Can intra‐specific genetic variation in arbuscular mycorrhizal fungi (Glomus etunicatum) affect a mesophyll‐feeding herbivore (Tupiocoris notatus Distant)?

Abstract.  1. Arbuscular mycorrhizal fungal (AMF) infection can have negative, positive or neutral effects on insect herbivore populations, but patterns are difficult to predict.
2. Intra-specific genetic variation in nutrient uptake ability between fungal isolates may also have indirect effects on insect herbivores due to changes in plant quality. In preliminary studies mirid ( Tupiocoris notatus ) populations were significantly reduced on tobacco ( Nicotiana rustica ) colonised by AMF but it was unknown if same-species fungal isolates differed in their effect.
3. An experiment was performed as a first test of the effect of intra-specific genetic variation in the mycorrhizal fungus Glomus etunicatum on mirid nymphal population structure, dynamics, and growth rate.
4. Mirid nymphal populations were lower on mycorrhizal fungal-infected plants. Population size, however, did not differ between the mycorrhizal isolates. While no statistical difference in population between isolates was found, one isolate consistently had 1.7–2.4 times lower mirid populations compared with the controls, indicating that the magnitude of effect is different between mycorrhizal isolates.
5. The significantly negative effect of AMF on mirid populations likely resulted from AMF-induced changes in plant quality (e.g. increased defence). This study lends further support to recent demonstrations that below-ground symbionts significantly influence above-ground processes. In addition, mycorrhizal fungi can affect insect population structure, which may have consequences for future herbivory.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Arbuscular mycorrhizal fungi reduce growth and infect roots of the non‐host plant Arabidopsis thaliana

The arbuscular mycorrhizal (AM) symbiosis is widespread throughout the plant kingdom and important for plant nutrition and ecosystem functioning. Nonetheless, most terrestrial ecosystems also contain a considerable number of non‐mycorrhizal plants. The interaction of such non‐host plants with AM fungi (AMF) is still poorly understood. Here, in three complementary experiments, we investigated whether the non‐mycorrhizal plant Arabidopsis thaliana, the model organism for plant molecular biology and genetics, interacts with AMF. We grew A. thaliana alone or together with a mycorrhizal host species (either Trifolium pratense or Lolium multiflorum) in the presence or absence of the AMF Rhizophagus irregularis. Plants were grown in a dual‐compartment system with a hyphal mesh separating roots of A. thaliana from roots of the host species, avoiding direct root competition. The host plants in the system ensured the presence of an active AM fungal network. AM fungal networks caused growth depressions in A. thaliana of more than 50% which were not observed in the absence of host plants. Microscopy analyses revealed that R. irregularis supported by a host plant was capable of infecting A. thaliana root tissues (up to 43% of root length colonized), but no arbuscules were observed. The results reveal high susceptibility of A. thaliana to R. irregularis, suggesting that A. thaliana is a suitable model plant to study non‐host/AMF interactions and the biological basis of AM incompatibility.     

Plant genotype and the preference and performance of herbivores: cultivar affects apple resistance to the florivorous weevil Anthonomus pomorum

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