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.     

Microbes in Helicoverpa armigera oral secretions contribute to increased senescence around plant wounds

1. Plants have long been exposed to insect herbivore attack. Crucial to the plant's ability to defend itself is its ability to identify specific signals associated with attacking insects. Distinctive chemical cues, such as those associated with chewing insect oral secretions (OS), activate targeted defence responses to chewing insect herbivores. 2. Herbivore-associated cues can be complicated by the fact that many herbivores form associations with microbes that produce their own specific signals, which may induce alternative defence processes. 3. Here we report that OS of the global pest, the cotton bollworm (Helicoverpa armigera), induce senescence around wounds in Brachypodium distachyon leaves. Crude OS activate greater levels of senescence than OS with reduced microbial abundance or mechanical wounding alone. Nonetheless, plants closed mechanical wounds more rapidly when treated with H. armigera OS regardless of the microbial component. 4. This study concludes that H. armigera OS can activate senescence and wound closure in plant tissues and that microbes within OS have an important role in shaping plant-herbivore interactions through additional increases in senescence.     

An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.     

Wound and insect‐induced jasmonate accumulation in carnivorous Drosera capensis: two sides of the same coin

Carnivorous sundew plants catch and digest insect prey for their own nutrition. The sundew species Drosera capensis shows a pronounced leaf bending reaction upon prey capture in order to form an ‘outer stomach’. This formation is triggered by jasmonates, phytohormones typically involved in defence reactions against herbivory and wounding. Whether jasmonates still have this function in D. capensis in addition to mediating the leaf bending reaction was investigated here. Wounded, insect prey‐fed and insect‐derived oral secretion‐treated leaves of D. capensis were analysed for jasmonates (jasmonic acid, JA; jasmonic acid‐isoleucine conjugate, JA‐Ile) using LC‐MS/MS. Prey‐induced jasmonate accumulation in D. capensis leaves was persistent, and showed high levels of JA and JA‐Ile (575 and 55.7 pmol·g·FW^?1, respectively), whereas wounding induced a transient increase of JA (maximum 500 pmol·g·FW^?1) and only low (3.1 pmol·g·FW^?1) accumulation of JA‐Ile. Herbivory, mimicked with a combined treatment of wounding plus oral secretion (W+OS) obtained from Spodoptera littoralis larvae induced both JA (4000 pmol·g·FW^?1) and JA‐Ile (25 pmol·g·FW^?1) accumulation, with kinetics similar to prey treatment. Only prey and W+OS, but not wounding alone or OS, induced leaf bending. The results indicate that both mechanical and chemical stimuli trigger JA and JA‐Ile synthesis. Differences in kinetics and induced jasmonate levels suggest different sensing and signalling events upon injury and insect‐dependent challenge. Thus, in Drosera, jasmonates are still part of the response to wounding. Jasmonates are also employed in insect‐induced reactions, including responses to herbivory and carnivory.     

Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores

Drought events are predicted to increase due to climate change, yet consequences for plant–insect interactions are only partially understood. Drought‐mediated interactions between herbivores and their host plants are affected by a combination of factors, including characteristics of the affected plant, its associated herbivore and of the prevailing drought. Studying the effect of these factors in combination may provide important insight into plant and herbivore responses to drought. We studied drought effects on plant resistance to two leaf‐chewing herbivores by considering differing growth conditions, plant chemistry and insect responses in concert. We exposed Alliaria petiolata plants from several wild populations to different intensities of intermittent drought stress and quantified drought‐mediated changes in plant chemistry. Simultaneously, we assessed behavior (feeding preference) and performance of two lepidopteran herbivores: Pieris brassicae, a specialist, and Spodoptera littoralis, a generalist. Drought led to lowest concentrations of secondary defense compounds in severely stressed plants, without affecting total nitrogen content. Additionally, drought evoked opposite patterns in feeding preferences (plant palatability) between the herbivore species. Pieris brassicae consumed most of well‐watered plants, while S. littoralis preferred severely drought‐stressed plants. Hence, feeding preferences of S. littoralis reflected changes in plant secondary chemistry. Contrary to their feeding preference, P. brassicae performed better on drought‐stressed than on well‐watered plants, with faster development and higher attained pupal mass (plant suitability). Spodoptera littoralis showed retarded development in all treatments. In conclusion, drought caused plant secondary defense compounds to decrease consistently across all studied plant populations, which evoked contrasting feeding preferences of two herbivore species of the same feeding guild. These results suggest herbivore specificity as a possible explanation for herbivore responses to drought and emphasize the importance of herbivore characteristics such as feeding specialization in understanding and predicting consequences of future drought events.     

Asymmetric effects of a leaf‐chewing herbivore on aphid population growth

1. Plant responses to herbivory are often specific to the feeding guild of the attacking herbivore. These phytochemical responses to herbivore damage can affect herbivore performance and activity. Comprehensive studies on the ecological consequences of multi‐herbivore plant interactions are key to understanding plant–herbivore community dynamics. 2. This study examined how feeding damage by co‐occurring herbivores from separate feeding guilds, Myzus persicae (Sulzer), a sucking herbivore, and Leptinotarsa decemlineata (Say), a chewing herbivore, alter plant chemistry and indirectly affect herbivore performance. Performance was measured when each insect fed on plants individually, sequentially, or simultaneously in laboratory and field experiments. Phytohormone and glycoalkaloid content were measured for each feeding sequence to evaluate plant responses to herbivory by each guild. Mid‐season and end‐of‐season tuber yield were evaluated in the field study. 3. Damage by L. decemlineata negatively impacted M. persicae performance in both laboratory and field settings. Damage by M. persicae did not affect L. decemlineata performance in laboratory assays. However, L. decemlineata performance was positively affected by M. persicae herbivory in the field, but this effect was temporary. Although phytohormones and plant defences varied across treatments, they provide little resolution on interaction outcomes. 4. These results confirm that the presence of multiple feeding guilds on a single plant can affect these chewing and sucking herbivores differentially, but given the variability in our phytochemical analyses compared with other studies, the mechanism remains unclear. The study's findings show that aphids are negatively affected by chewing herbivores across systems, while aphids temporarily affected beetles positively.     

An ecogenomic analysis of herbivore‐induced plant volatiles in Brassica juncea

Upon herbivore feeding, plants emit complex bouquets of induced volatiles that may repel insect herbivores as well as attract parasitoids or predators. Due to differences in the temporal dynamics of individual components, the composition of the herbivore‐induced plant volatile (HIPV) blend changes with time. Consequently, the response of insects associated with plants is not constant either. Using Brassica juncea as the model plant and generalist Spodoptera spp. larvae as the inducing herbivore, we investigated herbivore and parasitoid preference as well as the molecular mechanisms behind the temporal dynamics in HIPV emissions at 24, 48 and 72 h after damage. In choice tests, Spodoptera litura moth preferred undamaged plants, whereas its parasitoid Cotesia marginiventris favoured plants induced for 48 h. In contrast, the specialist Plutella xylostella and its parasitoid C. vestalis preferred plants induced for 72 h. These preferences matched the dynamic changes in HIPV blends over time. Gene expression analysis suggested that the induced response after Spodoptera feeding is mainly controlled by the jasmonic acid pathway in both damaged and systemic leaves. Several genes involved in sulphide and green leaf volatile synthesis were clearly up‐regulated. This study thus shows that HIPV blends vary considerably over a short period of time, and these changes are actively regulated at the gene expression level. Moreover, temporal changes in HIPVs elicit differential preferences of herbivores and their natural enemies. We argue that the temporal dynamics of HIPVs may play a key role in shaping the response of insects associated with plants.     

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.

     

Herbivore perception decreases photosynthetic carbon assimilation and reduces stomatal conductance by engaging 12‐oxo‐phytodienoic acid,mitogen‐activated protein kinase 4 and cytokinin perception

Herbivory‐induced changes in photosynthesis have been documented in many plant species; however, the complexity of photosynthetic regulation and analysis has thwarted progress in understanding the mechanism involved, particularly those elicited by herbivore‐specific elicitors. Here, we analysed the early photosynthetic gas exchange responses in Nicotiana attenuata plants after wounding and elicitation with Manduca sexta oral secretions and the pathways regulating these responses. Elicitation with M. sexta oral secretions rapidly decreased photosynthetic carbon assimilation (A_C) in treated and systemic (untreated, vascularly connected) leaves, which were associated with changes in stomatal conductance, rather than with changes in Rubisco activity and 1‐5 ribulose‐1,5‐bisphosphate turnover. Phytohormone profiling and gas exchange analysis of oral secretion‐elicited transgenic plants altered in phytohormone regulation, biosynthesis and perception, combined with micrografting techniques, revealed that the local photosynthetic responses were mediated by 12‐oxo‐phytodienoic acid, while the systemic responses involved interactions among jasmonates, cytokinins and abscisic acid signalling mediated by mitogen‐activated protein kinase 4. The analysis also revealed a role for cytokinins interacting with mitogen‐activated protein kinase 4 in CO₂‐mediated stomatal regulation. Hence, oral secretions, while eliciting jasmonic acid‐mediated defence responses, also elicit 12‐oxo‐phytodienoic acid‐mediated changes in stomatal conductance and A_C, an observation illustrating the complexity and economy of the signalling that regulates defence and carbon assimilation pathways in response to herbivore attack.     

Response of Brassica oleracea to temporal variation in attack by two herbivores affects preference and performance of a third herbivore

1. Plants are frequently under attack by multiple insect herbivores, which may interact indirectly through herbivore‐induced changes in the plant's phenotype. The identity, order, and timing of herbivore arrivals may influence the outcome of interactions between two herbivores. How these aspects affect, in turn, subsequently arriving herbivores that feed on double herbivore‐induced plants has not been widely investigated. 2. This study tested whether the order and timing of arrival of two inducing herbivores from different feeding guilds affected the preference and performance of a subsequently arriving third herbivore, caterpillars of Mamestra brassicae L. (Lepidoptera: Noctuidae). Aphids [Brevicoryne brassicae L. (Hemiptera: Aphididae)] and caterpillars [Plutella xylostella L. (Lepidoptera: Yponomeutidae)] were introduced onto wild Brassica oleracea L. (Brassicaceae) plants in different sequences and with different arrival times. The effects of these plant treatments on M. brassicae caterpillars were assessed in pairwise preference tests and no‐choice performance tests. 3. The caterpillars of M. brassicae preferred to feed from undamaged plants rather than double herbivore‐induced plants. Compared with undamaged plants, they preferred plant material on which aphids had arrived first followed by caterpillars, whereas they avoided plant material with the reverse order of herbivore arrival. Performance of the caterpillars increased with increasing arrival time between herbivore infestations in double herbivore‐induced plants. Although M. brassicae grew faster on plants induced by aphids than on those induced by caterpillars alone, its performance was not affected by the order of previous herbivore arrival. 4. These results imply that the timing of colonisation by multiple herbivores determines the outcome of plant‐mediated herbivore–herbivore interactions.     

Effects of non-native <Emphasis Type="Italic">Spartina patens</Emphasis> on plant and sediment organic matter carbon incorporation into the local invertebrate community

The cycling of organic matter through food webs is a fundamental process that may be altered by the invasion of non-indigenous plants. We explored consequences of the invasion of non-indigenous Spartina patens to the composition of soil organic matter (SOM) and to detritivore and herbivore diets in the upper salt marsh within Corrubedo National Park, northwest Spain. We tested for the incorporation of S. patens carbon (C) into SOM and by detritivores and herbivores using stable isotope analysis, focusing primarily on detritivorous enchytraeid oligochaetes and herbivorous insects. Stable isotope results indicated that C derived from S. patens has been incorporated into SOM. Elevated densities of enchytraeids in stands of S. patens, and their incorporation of C derived from this plant, suggested that dense patches of S. patens may facilitate detritivore populations. In contrast, although insect herbivores used S. patens as habitat, there was little isotopic evidence for the widespread incorporation of S. patens-derived C by these consumers. The population and dietary response of enchytraeids to S. patens suggests that S. patens invasion could indirectly influence soil processes and pathways mediated by detritivore activity (e.g., soil respiration rates, nutrient retention and transformation, energy flow). The loss of food resources to insect herbivores alters local food webs. However, insect herbivores may move and feed on native plants elsewhere. As a result, insect populations may be less immediately impacted than soil detritivore populations by S. patens. Our study suggests that the influences of S. patens invasion extend beyond the more obvious changes in native plant abundance, to include differing responses in the cycling of organic matter between detritivore and insect herbivore food web pathways.     

Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference

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The direct and indirect effects of fire on the assembly of insect herbivore communities: examples from the Florida scrub habitat

Disturbance is a major source of spatial and temporal heterogeneity. In fire-maintained systems, disturbance by fire is often used as a management tool to increase biological diversity, restore degraded habitats, and reduce pest outbreaks. Much attention has been given to how plant communities recover from fire, but relatively few studies have examined post-fire responses of higher order species, such as insect herbivores. Because dynamic feedbacks occur between plants and their consumers, which can in turn influence the response of the entire ecosystem, incorporating higher trophic level responses into our understanding of the effects of fire is essential. In this study, we used structural equation modeling (SEM) to tease apart the direct and indirect effects of fire on insect herbivore assemblages found on three common oak species in the Florida scrub (Quercus inopina, Q. chapmanii, and Q. geminata). We investigated how fire affected herbivore abundance, richness, and community composition both directly and indirectly through environmental heterogeneity at different spatial scales (e.g., leaf quality, plant architecture, and habitat structure). We also investigated how seasonality and landscape heterogeneity influenced post-fire responses of insect herbivores and whether fire effects on herbivore assemblages varied among different host plants. Our general findings were that fire effects were (1) largely indirect, mediated through habitat structure (although direct fire effects were observed on Q. inopina herbivores), (2) non-linear through time due to self-thinning processes occurring in the scrub habitat, and (3) varied according to herbivore assemblage as a result of differences in the composition of species in each herbivore community. To the best of our knowledge, this is the first comprehensive study to examine how fire influences the assembly of insect herbivore communities through both direct and indirect pathways and at multiple spatial scales.