Every cloud has a silver lining: Moderate plant water stress positively impacts development, immunity, and gut microbiota of a specialist herbivore (original) (raw)
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Arthropod-Plant Interactions, 2012
Water availability and plant community composition alter plant nutrient availability and the accumulation of plant defence compounds therefore having an impact on herbivore performance. Combined effects of drought stress and plant community composition on leaf chemicals and herbivore performance are largely unexplored. The objective of our study was, therefore, to find out the impact of extreme drought and of plant community composition on plant-herbivore interactions. Larvae of the generalist butterfly Spodoptera littoralis were reared on leaves of the grass Holcus lanatus which was grown in experimental communities, differing in species-and functional group richness. These communities were either subjected to extreme drought or remained under ambient climatic conditions. Drought decreased relative water content, soluble protein content, nitrogen and total phenol content and increased the content of carbohydrates in the grass. As a consequence, the larvae feeding on drought-exposed plants revealed a longer larval stage, increased pupal weight and higher adult eclosion rates. Plant community composition mainly caused changes to the defensive compounds of the grass, but also marginally affected protein and carbohydrate content. Larvae feeding on species-richest communities without legumes showed the highest mortality. Our findings imply that climate change that is projected to increase the frequency of severe droughts, as well as alter plant community compositions, is likely to affect arthropod-plant interactions through an alteration of leaf chemicals.
Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores
Oikos, 2011
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. ese 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.
Journal of Animal Ecology
1. Widespread population declines have been reported for diverse Mediterranean butterflies over the last three decades, and have been significantly associated to increased global change impacts. The specific landscape and climatic drivers of these declines remain uncertain for most declining species. 2. Here we analyse whether plastic phenotypic traits of a model butterfly species (Pieris napi) perform as reliable biomarkers of vulnerability to extreme temperature impacts in natural populations, showing contrasting trends in thermally exposed and thermally buffered populations. 3. We also examine whether improved descriptions of thermal exposure of insect populations can be achieved by combining multiple information sources (i.e. integrating measurements of habitat thermal buffering, habitat thermal amplification, host plant transpiration, and experimental assessments of thermal death time (TDT), thermal avoidance behaviour (TAB) and thermally induced trait plasticity). These integrative analyses are conducted in two demographically declining and two non-declining populations of P. napi. 4. The results show that plastic phenotypic traits (butterfly body mass and wing size) are reliable biomarkers of population vulnerability to extreme thermal conditions. Butterfly wing size is strongly reduced only in thermally exposed populations during summer drought periods. Lab rearing of these populations documented reduced wing size due to Accepted Article This article is protected by copyright. All rights reserved. significant negative effects of increased temperatures affecting larval growth. We conclude that these thermal biomarkers are indicative of the population vulnerability to increasing global warming impacts, showing contrasting trends in thermally exposed and buffered populations. 5. Thermal effects in host plant microsites significantly differ between populations, with stressful thermal conditions only effectively ameliorated in mid-elevation populations. In lowland populations we observe a six-fold reduction in vegetation thermal buffering effects, and larval growth occurs in these populations at significantly higher temperatures. Lowland populations show reduced host plant quality (C/N ratio), reduced leaf transpiration rates and complete aboveground plant senescence during the peak of summer drought. Amplified host plant temperatures are observed in open microsites, reaching thermal thresholds that can affect larval survival. 6. Overall, our results suggest that butterfly population vulnerability to long-term drought periods is associated to multiple co-occurring and interrelated ecological factors, including limited vegetation thermal buffering effects at lowland sites, significant drought impacts on host plant transpiration and amplified leaf surface temperature, as well as reduced leaf quality linked to the seasonal advance of plant phenology. Our results also identify multi-annual summer droughts affecting larval growing periods as a key driver of the recently reported butterfly population declines in the Mediterranean biome.
Beneficial microbes in a changing environment: are they always helping plants to deal with insects?
Functional Ecology, 2013
Plants have a complex immune system that defends them against attackers (e.g. herbivores and microbial pathogens) but that also regulates the interactions with mutualistic organisms (e.g. mycorrhizal fungi and plant growth-promoting rhizobacteria). Plants have to respond to multiple environmental challenges, so they need to integrate both signals associated with biotic and abiotic stresses in the most appropriate response to survive. 2. Beneficial microbes such as rhizobacteria and mycorrhizal fungi can help plants to 'deal' with pathogens and herbivorous insects as well as to tolerate abiotic stress. Therefore, beneficial microbes may play an important role in a changing environment, where abiotic and biotic stresses on plants are expected to increase. The effects of beneficial microbes on herbivores are highly context-dependent, but little is known on what is driving such dependency. Recent evidence shows that abiotic stresses such as changes in soil nutrients, drought and salt stress, as well as ozone can modify the outcome of plant-microbe-insect interactions. 3. Here, we review how abiotic stress can affect plant-microbe, plant-insect and plantmicrobe-insect interactions, and the role of the network of plant signal-transduction pathways in regulating such interactions. 4. Most of the studies on the effects of abiotic stress on plant-microbe-insect interactions show that the effects of microbes on herbivores (positive or negative) are strengthened under stressful conditions. We propose that, at least in part, this is due to the crosstalk of the different plant signalling pathways triggered by each stress individually. By understanding the cross-regulation mechanisms we may be able to predict the possible outcomes of plantmicrobe-insect interactions under particular abiotic stress conditions. We also propose that microbes can help plants to deal with insects mainly under conditions that compromise efficient activation of plant defences. 5. In the context of global change, it is crucial to understand how abiotic stresses will affect species interactions, especially those interactions that are beneficial for plants. The final aim of this review is to stimulate studies unravelling when these 'beneficial' microbes really benefit a plant.
Plant-mediated effects of drought stress on host preference and performance of a grass miner
Oikos, 2005
. Plant-mediated effects of drought stress on host preference and performance of a grass miner. Á/ Oikos 108: 371 Á/385. The plant stress hypothesis predicts that environmental stress increases the suitability of plants as food for herbivores, especially for senescence feeders. Yet, performance is enhanced only at moderate stress intensities in several herbivores. Even more paradoxically, a large number of insect species prefer and perform better on vigorously growing plants. In order to test plant stress theory, we conducted a laboratory experiment in which the influence of plant water stress on host preference and the performance of the grass miner Chromatomyia milii was studied. We imposed a gradient of stress intensities, i.e. 25, 50, 75, 150, and 300-ml weekly-administered water per grass pot, in order to study the full range of responses of C. milii to water stressed plants. Plant stress intensity was quantified by measuring individual plant mass, foliar water content and the concentration of the photosynthetic pigments chlorophyll a and b. Plant mass had decreased from the 150 and 300-ml treatments to the lowest water treatment at the end of our experiment, which was mainly a result of a reduction in leaf area and leaf number. Foliar water content was clearly negatively affected by water shortage. Chlorophyll a and b also decreased with water shortage. Finally, the stress intensity measurements showed that plants acclimated to water stress conditions throughout the experiment. Feeding and oviposition preference of C. milii was positively related to water supply. No larvae survived on two lowest water treatments and only 38% survived on the 75-ml treatment, while more than 80% survived on the 150 and the 300-ml treatments. Offspring development time was longer on the 75-ml treatment than on the 150 and the 300-ml treatments. We also evaluated the mechanisms that could explain the response of C. milii to water stressed plants. Although no relationship between water treatment and foliar amino acid concentration was found, we observed significantly higher foliar protein concentrations in the 25 and the 50-ml treatments. This supports the hypothesis that abiotic stress causes an increase of nitrogenous compounds in plants. Leaf senescence following self-pruning, a process by which H. lanatus plants acclimate to drought conditions, was responsible for the dramatically high offspring mortality on the water stressed plants. The shape of the plant stress intensity Á/herbivore response relationship showed strong variation and depended both on the type of plant stress intensity measure and herbivore response variable involved. Yet, all relationships showed a monotonic increase of herbivore preference and performance with decreasing plant stress intensity. This indicates that C. milii prefers and performs better on vigorously growing plants. We found no support for an increased herbivore performance on moderately or severely stressed plants.
Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet
Frontiers in microbiology, 2016
Herbivores possess many counteradaptations to plant defenses, and a growing body of research describes the role of symbiotic gut bacteria in mediating herbivorous diets among insects. However, persistent bacterial symbioses have not been found in Lepidoptera, despite the fact that perhaps 99% of the species in this order are herbivorous. We surveyed bacterial communities in the guts of larvae from 31 species of lycaenid butterflies whose caterpillars had diets ranging from obligate carnivory to strict herbivory. Contrary to our expectations, we found that the bacterial communities of carnivorous and herbivorous caterpillars do not differ in richness, diversity, or composition. Many of the observed bacterial genera are commonly found in soil and plant surfaces, and we detected known homopteran endosymbionts in the guts of homopterophagous species, suggesting that larvae acquire gut bacteria from their food and environment. These results indicate that lycaenid butterflies do not rely ...
Functional Ecology, 2015
1. Climate change models predict more extreme rainfall patterns, ranging from droughts to deluges, which will inevitably affect primary productivity in many terrestrial ecosystems. Insects within the ecosystem, living above-and below-ground, may modify plant responses to water stress. For example, some functional groups improve soil conditions via resource provision, potentially alleviating water stress. Enhanced resource provision may, however, render plants more susceptible to herbivores and negate beneficial effects. 2. Using a model system, we tested how plants (Brassica oleracea) responded to drought, ambient and increased precipitation scenarios when interacting with both a soil conditioning ecosystem engineer (dung beetles; Bubas bison) and an above-ground herbivore, the major crop pest diamondback moth (Plutella xylostella). 3. Dung beetles enhanced soil water retention by 10% and promoted growth in plants subjected to drought by 280%, relieving the impacts of water stress on plants. Under drought conditions, plants grown with dung beetles had c. 30% more leaves and were over twice as tall as those without dung beetles. Dung beetles produced a 2Á7-fold increase in nitrogen content and more than a threefold increase in carbon content of the shoots, though shoot concentrations of nitrogen and carbon were unchanged. Carbon concentrations in roots, however, were increased by dung beetles under both ambient and increased precipitation regimes. 4. Increased precipitation reduced root and shoot nitrogen concentrations by 16% and 30%, relative to plants under ambient regimes, respectively, most likely due to dilution effects of increased plant growth under increased precipitation. Soil carbon and nitrogen concentrations were largely unaffected. 5. While dung beetles enhanced plant growth and nitrogen content in plants experiencing drought, the anticipated increase in plant suitability to herbivores did not arise, possibly because shoot nitrogen concentrations and C:N ratio were unaffected. 6. To our knowledge, this is the first report of an insect ecosystem engineer alleviating the effects of predicted drought events on plants via physical manipulation of the soil matrix. Moreover, their effects did not change plant suitability to an above-ground herbivore, pointing to potential beneficial role for insect ecosystem engineers in climate change adaptation and crop protection.
Impacts of a millennium drought on butterfly faunal dynamics
Climate Change Responses, 2018
Background: Climate change is challenging plants and animals not only with increasing temperatures, but also with shortened intervals between extreme weather events. Relatively little is known about diverse assemblages of organisms responding to extreme weather, and even less is known about landscape and life history properties that might mitigate effects of extreme weather. Our aim was to address this knowledge gap using a multi-decadal dataset of 163 butterfly species that recently experienced a millennium-scale drought. To understand faunal dynamics in the context of the millennium drought, we investigated the behavior of phenology (including date of first flight), species richness and diversity indices through time at 10 study sites spanning an elevational gradient. Linear models were developed to understand the differential sensitivity of butterflies to climate at low and high elevations. Results: Dates of first flight advanced across the elevational gradient during the drought, leading to an overall expansion of the flight window at low elevations and a compression of the flight window in the mountains. The number of species observed per year increased at lower elevations but decreased at higher elevations, apparently as a consequence of extreme sensitivity to hot and dry conditions. Conclusion: Montane populations may be more sensitive to climatic extremes than expected based on availability of microclimates and spatial heterogeneity, while low-elevation populations (despite existing in degraded habitats) are buffered by life history plasticity.
Oecologia, 2015
One of the main abiotic stresses that strongly affects plant survival and the primary cause of crop loss around the world is drought. Drought stress leads to sequential morphological, physiological, biochemical and molecular changes that can have severe effects on plant growth, development and productivity. As a consequence of these changes, the interaction between plants and insects can be altered. Using cultivated Brassica oleracea plants, the parasitoid Microplitis mediator and its herbivorous host Mamestra brassicae, we studied the effect of drought stress on (1) the emission of plant volatile organic compounds (VOCs), (2) plant hormone titres, (3) preference and performance of the herbivore, and (4) preference of the parasitoid. Higher levels of jasmonic acid (JA) and abscisic acid (ABA) were recorded in response to herbivory, but no significant differences were observed for salicylic acid (SA) and indole-3-acetic acid (IAA). Drought significantly impacted SA level and showed a...